AMER. ZOOL., 31:17-33 (1991)
Antarctic Sea Ice Biota1
DAVID L. GARRISON
Institute of Marine Sciences, University of California, Santa Cruz, California 95064
SYNOPSIS. The sea ice surrounding Antarctica provides an extensive habitat for organisms ranging in size from bacteria to marine birds and mammals. Historically, most of the
ecological work on the ice biota has focused in the nearshore land-fast ice. Only in the
last decade have there been comparable studies in the deep-water pack ice regions. These
studies have indicated that there are fundamental differences in structural and physical
characteristics of fast and pack ice that are a result of differing physical regimes in nearshore and oceanic regions. Other physical processes act to create heterogeneity within
the ice habitat that can range from geographic and regional scales of patchiness to a
pronounced vertical gradient within ice floes. The conspicuous patterns in the distribution
of the ice biota can be explained largely by these physical processes.
Over 200 species have been reported living on, in, or in association with Antarctic sea
ice. The ice biota includes bacteria, a variety of algae, heterotrophic protozoans and small
metazoans. The diatom assemblages are the only taxonomic group that is known well
enough to make comparisons among the various habitats. Studies by a number of workers
suggest some specific diatom assemblages along with occurrence of species that are widelydistributed in both ice and plankton. Ice may also serve as a temporary habitat for species
that also comprise planktonic communities, so that providing a "seed population" for ice
edge plankton blooms may be an important role of the ice biota. Trophic interactions
among organisms in ice suggest that the ice assemblage is a true community with a welldeveloped microbial food web. The ice microbial community may be an important part
of the Antarctic marine food web because large consumers from the adjacent planktonic
and benthic communities appear to feed on the ice biota.
ing seasonal observations, has focused on
The sea ice surrounding Antarctica is land-fast ice near one of the Antarctic
one of the prominent features of the south- research stations; this has led to the the
ern ocean. Ice provides habitat for a vari- biased view that conditions in these shalety of marine mammals and birds, and the low-water environments are typical
surfaces and interstices of the ice are a throughout the ice-covered regions. Recent
microhabitat colonized by bacteria, algae, studies {e.g., see Garrison etai, 1986), howheterotrophic protozoans and small meta- ever, have suggested that the physical and
zoans. The microbial assemblage associ- biological regimes differ in the land-fast
ated with ice is particularly important and pack ice regions. Although this theme
because, along with plankton, it forms the is developed throughout this review, this
is still an emerging hypothesis that requires
energy base of the marine food web.
more extensive documentation.
Studies of the ice biota had an early start
Horner's (19856) volume, Sea Ice Biota,
in Antarctic waters. For example, the disprovides
a comprehensive review of studies
coloration of ice floes by algae was
described by Hooker (1847) over 140 years in both Arctic and Antarctic regions
ago. In spite of this early beginning, sig- through the early 1980s. However, much
nificant ecological studies did not begin of the work in the Antarctic pack ice regions
until the late 1950s (see Horner, 1985a and is even more recent. Moreover, with the
Garrison et al., 1986 for recent reviews). exception of bacteria (Sullivan, 1985), until
Because of the logistical difficulty of work- our studies in the Weddell Sea, there has
ing in the remote pack ice regions, much been little information about the microhetof the research, particularly studies involv- erotrophic members of the ice biota (e.g.,
Garrison et al., 1986; Garrison and Buck,
1988, 1989a; also see Carey, 1985). While
1
From the Symposium on Antarctic Marine Biology
including some historical and background
presented at the Annual Meeting of the American
information in this review, I have attempted
Society of Zoologists, 27-30 December 1988, at San
to focus on the findings from recent studies
Francisco, California.
INTRODUCTION
17
18
DAVID L. GARRISON
.. .
under-ice
platelet layer
bottom ice
layer
internal banded
layers
FIG. 1. A diagrammatic representation of the sea ice surrounding Antarctica. The microbial habitats are
discussed in the text. Figure from Garrison et al. (1986) with permission from BioScience.
to provide a more comprehensive picture
of the distribution, composition and role
of the ice biota in the Antarctic marine
system.
T H E ENVIRONMENT
The sea ice habitat
Sea ice forms an extensive habitat in the
southern ocean with ice covering >20 x
106 km2 of the sea surface in the austral
winter and contracting to <4 x 106 km2
in the summer (Zwally et al., 1983; Foster,
1984). In some regions, such as the Weddell and Bellingshausen seas, a considerable amount of ice persists throughout the
summer. The survival of ice floes throughout the summer melting period results in
some multiyear ice, but in most regions of
the Antarctic, sea ice is an ephemeral,
annual habitat. The ice-covered regions can
be divided into a zone of land-fast ice in
the shallow areas adjacent to the continent
and the free-floating pack ice which extends
into the deep-water regions (Fig. 1).
Although there is a continuum between
fast- and pack ice regions, the physical
regimes differ in the coastal and deep-water
environments, which results in ice floes
which differ in their characteristics as biological habitats.
Physical and chemical characteristics
In most ecological studies it is of fundamental importance to examine the physical and chemical characteristics of the
environment in order to understand the
biological feature. This is particularly true
of sea ice because the ice habitat is largely
structured by physical processes. It is now
becoming apparent that the establishment
of biological organisms in ice and their subsequent growth and development is related
to physical processes.
Some of the important physical and biological characteristics of sea ice are determined during ice formation. In the initial
stages of freezing, ice crystals form in the
water column, float to the surface and
accumulate as grease ice. As the freezing
process continues, ice crystals coalesce to
form nilas or sheet ice under calm conditions, or pancake ice if there is any wave
action. This newly-forming ice is characterized by a random orientation of ice crys-
ANTARCTIC ICE BIOTA
19
tals in the ice matrix and is often referred lished ice floes (e.g., Bunt, 1963). These
to asfrazil ice (see Weeks and Ackley, 1982 platelet layers are believed to form as water
for a more comprehensive discussion of ice circulating under ice shelves is supercooled
formation and growth). One important allowing ice crystals to form below the surproperty of frazil ice is that it can harvest face (Maykut, 1985; Lange, 1988). Icefloes
and concentrate particulate material from may be depressed by the accumulation of
the underlying water, so that organisms snow (Meguro, 1962; Ackley, 1988) or as
may be highly concentrated even in very the result of pressure ridge formation
young sea ice (e.g., Garrison et al., 1983). (Ackley, 1985), that allows sea water to
Once the sea surface is ice covered, addi- flood the floes and to form a layer of infiltional heat loss to the atmosphere must take tration ice at the snow-ice interface. This
place through the ice sheet, and ice for- layer seems to be more common on pack
mation takes place at the ice-water inter- ice floes than in land-fast ice and may vary
face. Under these conditions the crystals from region to region with variations in
in the ice matrix assume a regular orien- snow fall, the amount of snow drift and the
tation, and this type of ice is referred to as extent of ice compression, which produces
congelation or columnar ice. Congelation ice pressure ridging (Ackley, 1985, 1988).
tends to reject particulate material during
On a much smaller scale, gradients in
ice formation, so that both the structural light, temperature and salinity produce
and biological characteristics of congela- marked vertical heterogeneity throughout
tion ice may be very different from those ice floes. Solar radiation falling on sea ice
of frazil ice (Clarke and Ackley, 1984).
is attenuated by snow, the ice itself and any
Differences in the physical regimes of biological organisms associated with ice,
oceanic and coastal areas result in large- and the light regime throughout ice floes
scale heterogeneity of the ice habitat. In can vary from one of high to low light
the pack ice regions, the wind-driven diver- depending on snow depth, ice thickness and
gence of ice floes maintains a considerable biological activity (Maykut, 1985; Sullivan
amount of open water, so that turbulent et al., 1984). The temperature differential
mixing, and consequently frazil ice pro- between air (often <—20°C in winter) and
duction, can be maintained (Weeks and seawater (-—1.9°C) results in a strong
Ackley, 1982; Clarke and Ackley, 1984). temperature gradient throughout ice floes.
Structural studies showing a predomi- Brine salinity varies inversely with tempernance of frazil ice in pack ice floes suggest ature and brine volume varies directly with
that accretion of frazil ice to existing floes temperature (Maykut, 1985), so that the
is the primary way ice floes grow in some osmotic environment as well as the volume
regions such as the Weddell Sea (e.g., Clarke of the microhabitat will vary throughout
and Ackley, 1984; Lange et al., 1989). In ice as the result of the temperature gracontrast, ice floes in some nearshore, fast dient. Kottmeier and Sullivan (1988) and
ice regions are mostly composed of con- Bartsch and Dieckmann (1988) have mea10°C
gelation ice, which may reflect the rela- sured low temperatures reaching
tively quite conditions of the coastal regions and corresponding elevated salinities of
(Gow et al., 1982). In addition, deforma- ~ 150%o in brine collected from the surface
tional events such as ice rafting, the for- of ice floes in winter; such conditions should
mation of pressure ridges and the break- be expected to influence biological activity
up of ice floes by sea-swell may be more and the distributions of organisms in ice
prevalent in the hydrographically dynamic (e.g., Meguro et al., 1967; Grossi and Sulpack ice region than in coastal areas (Ack- livan, 1985; Kottmeier and Sullivan, 1988).
ley, 1985; Ackley et al., 1986; Lange et al.,
Seasonal changes in ice as the result of
1989).
warming and melting also alter the charOther physical processes produce het- acteristics of the sea ice habitat. As temerogeneity of a more local scale. In near- peratures and brine volumes increase,
shore regions a layer of unconsolidated ice adjacent brine cells may fuse and flow
platelets often accumulates under estab- downward under the influence of gravity
20
DAVID L. GARRISON
(Weeks and Ackley, 1982; Maykut, 1985).
This brine drainage reduces the bulk salinity of ice and may produce millimeter to
centimeter sized brine drainage channels
throughout ice floes. These structural features alter the exchange between ice and
the underlying water, so summer ice and
multiyear floes (i.e., those surviving the
summer melting period) will differ in this
respect from younger ice floes.
SEA ICE COMMUNITIES
Distributions
Because of the pronounced heterogeneity of the ice habitat, it is not particularly
surprising that the biota associated with ice
is also patchy in abundance and occurrence. The distribution of algal assemblages has suggested several more-or-less
distinct microhabitats (Table 1; Fig. 1; also
see Horner et al., 1988). The occurrences
of the various microhabitats in ice can be
largely explained by the physical processes
discussed in the preceding section. For
example, the under-ice platelet layer and
its associated biota are mostly restricted to
nearshore regions where ice platelets form
(see Fig. 1). Other bottom-layer assemblages have been associated with the lower
20—30 cm of congelation ice, which predominates in fast ice floes (Garrison et al.,
1986). Internal communities, which occur
throughout pack ice floes, are thought to
be the result of the incorporation of organisms harvested from the water column by
frazil ice (Clarke and Ackley, 1984; Garrisons al., 1983, 1986). An internal banded
assemblage in some fast ice regions, however, appears to be the result of an autumn
bloom in the bottom layer of congelation
ice which is later entrapped as additional
ice is formed below it in winter ice (e.g.,
Hoshiai, 1977). Surface-layer assemblages
are thought to develop in a layer of infiltration ice produced by flooding (e.g.,
Meguro, 1962; Ackley, 1985, 1988), and
appear to be more common in pack ice. A
surface melt-pond assemblage in land-fast
ice at Casey station was reported by
McConville and Wetherbee (1983), but
surface melting is an unusual situation in
the Antarctic (see Horner et al., 1988).
A seasonal cycle of algal abundance in
land-fast ice, which may include both
autumn and spring blooms, has been
reported in several studies (see Horner
1985c for a review). The seasonal pattern
in pack ice is not well known. Measurements of chlorophyll a in internal assemblages in annual sea ice show little seasonal
variation (Garrison and Buck, 1989a). Surface-layer assemblages, however, appear to
develop to a seasonal maximum in the summer (Burkholder and Mandelli, 1965; Garrison and Buck, 1989a). There are some
obvious differences among the various
assemblages in how long they remain associated with ice. For example, the bottomlayer and platelet assemblages are lost in
the early stages of the seasonal melt cycle
(see Horner, 1985c), whereas those in
internal and surface-layer assemblages may
remain with ice floes for an extended
period. According to studies by Sullivan
andcoworkers (e.g., Kottmeier etal., 1987)
the cycles of bacterial abundance follow
those of the algae. The dynamics of other
microbial groups associated with ice are
still poorly known (Garrison and Buck,
1989a).
The biota
Over 200 taxa have been reported to live
in, on, or in association with Antarctic sea
ice (Table 2). For many of the microbial
groups, the number of species reported is
a reflection of the intensity of systematic
studies rather than a true representation
of diversity. A variety of terms such as epontic, "out of the sea," sympagic, "with ice,"
and cryophilic, "cold loving," have been used
to refer to the organisms associated with
ice (see Horner, 1985c and Horner et al.,
1988 for a more complete discussion of
terminology). Of these, "sympagic" is
probably a more generally correct term
because it carries no assumptions about the
source of the organisms or their physiological characteristics. Since the ice assemblage is now known to include organisms
from several trophic levels, which clearly
comprise an active food web (Garrison et
al., 1986; Garrison and Buck, 1989a), the
use of "community" to describe the ice
assemblage seems appropriate.
21
ANTARCTIC ICE BIOTA
TABLE 1. Ice algal assemblages in Antarctic sea ice.*
Assemblage
Specific nabitats
Surface layer
Pack ice: Infiltration
ice layer at snowice interface.
Flood ponds associated with pressure ridges.
Fast ice: Surface
meltpools.
Interior assemblage
Pack ice: Throughout ice floes comprised primarily
of frazil ice.
Fast ice: Autumn
blooms trapped
by growing congelation ice.
Fast ice: Brine channels in spring/
summer.
Location. Citations
Lutzow-Holm Bay: Meguro (1962); Fukushima and Meguro (1966). Antarctic Peninsula: Burkholder and Mandelli (1965). Weddell Sea: Garrison
and Buck (1989a); Ackley (1985);
Clarke and Ackley (1984).
Casey Station: McConville and Wetherbee (1983).
Weddell Sea: Ackley et al. (1978);
Clarke and Ackley (1984); Garrison
and Buck (1985, 1989a).
Sub-ice assemblage
Fast ice: Mats or
strands of algae
that extend below
established ice
floes.
Amphiprora kjellmanii, Chaetoceros neograale, Gymnodimum spp., misc. flagellates, Nitzschia dosterium, N.
curia, N. cylindrus, N. lineata, N. prolongatoides, N. turgiduloides, Phaeocystis pouchetn, Synedra spp., Thalasswsira gracilis, Tropidoneis fusiformis, T.
glaaalis
Nitzschia lineata, N. dosterium, N. obliquecostata, N.ritscheri,Plaeocystis
pouchetii
Amphiprora kjellemanii, Chaetoceros neogracile, Nitzschia angulata, N. dosterium, N. curta, N. cylindrus, N. neglecta, N. prolongatoides, N. subcurvata,
N. turgiduloides, Synedra sp., Tropidoneis fusiformis, T. glacialis
Syowa Station: Hoshiai (1977); Watanabeand Satoh (1987).
Casey Station: McConville and Wetherbee (1983).
Bottom layer assemblage
Fast ice: The lower
Casey, Mawson and Davis Stations:
~20 cm of congeMcConville and Wetherbee (1983).
lation ice.
McMurdo Sound: Bunt (1963); Grossi and Sullivan (1985); Grossi (1985).
Fast ice: Within an
accumulation of
ice platelets under
consolidated floes.
Characteristic species
McMurdo Sound: Bunt (1963); Grossi
(1985).
McMurdo Sound: Grossi (1985). Syowa
Station: Watanabe (1988). Casey,
Mawson and Davis Stations: McConville and Wetherbee (1983).
Amphiprora kufferathii, Berkeleya (Amphipleura sp.), Fragilaria islandica,
Nitzschia stellata, Pinnularia quadratrea v. constricta, Pleurosigma sp., Synedra sp.
Chaetoceros spp., Nitzschia dosterium, N.
curta, N. kerguelensis, Porosira pseudodenticulata, Thalassiosira antarctica
v. antarctica
Amphiprora kufferathii, Berkeleya rulilans, Entomoneis palisdosa v. hyperborea (Amphiprora), Nitzschia fngida, N.
lecointei, N. stellata, N. turgiduloides,
Synedra sp.
* Terminology referring to ice assemblages was modified from Homer et al. (1988). Characteristic species
were abstracted from Watanabe (1982, 1988); McConville and Wetherbee (1983); Grossi (1985); Grossi and
Sullivan (1985); Garrison and Buck (1985, 1989a). See Table 2 for authorities. Because summarizing species
assemblages from original sources was subjective, the "characteristic" species should be regarded as tentative.
Most of the studies of the ice community may also be abundant in ice (e.g., Watanahave focused on diatoms, which usually be, 1982; Garrison et al., 1987). The quesdominate the ice biota and are clearly the tion of whether diatoms rely on a resting
best known group associated with the ice. stage to overwinter in ice floes is unsettled.
Pennate species belonging to the Fragilar- Although a few of the diatoms found in ice
iopsis group (e.g., Nitzschia cylindrus and N.form resting spores, the most common specurta) are typical ice-associated forms (see cies (e.g., Nitzschia spp., see Table 2) do not
Tables 1 and 2), but several centric diatoms have a distinctive resting stage (Garrison
TABLE 2.
N
A summary of organisms reported from Antarctic sea ice including those linked to ice-based food webs.*
Pack
ice
Diatoms
C. oculus-iridis Ehrenberg
C. pyrenoidophorus Karsten
C radiatus Ehrenberg
C. rothii v. stelliger Frenguelli and Orlando
C. stella ris v. asteromphalus (Grunow) Jorgensen
Dactyliosolen antarcticus Castracane
D. tenuijunctus (Manguin) Priddle and Fryxell
Diplonesis sp.
Entomoneis paludosa v. hyperborea (Grunow) Poulin and
Cardinal
Eucampia antarctica (Castracane) Manguin
Fragilaria islandica v. adelme Manguin
Gomphonema intricatum Kutzing
Gyrosigma spp.
Haslea trompii (Cleve) Simonsen
Leptocyhndrus antarcticus
L. mediterranean (H. Peragallo) Hasle
Licmophora spp.
Melosira subhaylina
Navicula bicapitata Heiden and Kolbe
iV. cnophila (Castracane) DeToni
N. directa (Wm. Smith) Ralfs
N glaciei Van Heurck
Nitzschia angulata Hasle
N. castracanei Hasle
;V. closterium (Ehrenburg) W. Smith
N. curta (Van Heurck) Hasle
N. cylindrus (Grunow) Hasle
N. heimii (Manguin) Hasle
N. hybrida
N. frigida Grunow
N. kerguelensis (O'Meara) Hasle
N. lecotntei Van Heurck
N. hneata (Castracane) Hasle
N. lineola Cleve
N. neglecta Hustedt
Pack
ice
Landfast ice
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
a
+
+
S
r
+
o
J
7
[SON
Achnanthes spp.
Actinocyclus actinochilus (Ehrenberg) Simonsen
Amphiprora kjellmanii Cleve
A. kufferathii Manguin
Amphora spp.
A. antarctica Hustedt
Asteromphalus spp.
Auricula compacla (Hustedt) Medlin
Berkeleya rutilans (Trentepohl) Grunow
Biddulphia punctata Greville
Chaetoceros allanlicum Cleve
C. breve Schutt
C. bulbosum (Ehrenberg) Heiden
C. castracanei Karsten
C. convolutum Castracane
C. criophilum Castracane
C. curvisetum Cleve
C. debile Cleve
C. dichaeta Ehrenberg
C. flexuosum Manguin
C. neglectum Karsten
C. neogracile Van Landingham
C. pelagicum Cleve
C. pendulum Karsten
C. peruvianum Brightwell
C. simplex Ostenfelt
C. wighami Brightwell
Cocconeis spp.
C. fasciolata (Ehrenberg) Brown
C. costata Gregory
C. schuettii VanHeurck
Corethron criophilum Castracane
Cosrinodiscus asteromphalus Ehrenberg
C. oculoides Karsten
Landfast ice
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
TABLE 2. Continued.
Pack
ice
A', obliquecostata (Van Heurck) Hasle
N. pa lea
N. polans (Grunow)
A', prolongatoides Hasle
N. pseudonana Hasle
A',ritscheri(Hustedt) Hasle
N. slellala Manguin
N. subcurvata Hasle
A', sublineata Hasle
A', turgiduloides Hasle
A', vanheurckh (M. Peragallo) Hasle
Odontella weissjlogii (Grunow) Janisch
Pinnularia quadratarea v. biconstricta Oestrup
Pleurosigina sp.
P. directum Grunow
Porosira glacialis (Grunow) Jorgensen
P. pseudodenticulata (Hustedt) Jouse
Rhizosolenia alata Brightwell
Ft. alata f. inermis (Castracane) Hustedt
R. chunii Karsten
R. cylindnis Cleve
R. styliformis Brightwell
R. shrubsolei (Cleve) Van Heurck
R. truncata Karsten
Schimperiella antarctica Karsten
Stauronesis amphioxys Gregory
S. chacotii
Stellarima microtrias Hasle and Sims (Cosconodisciis
furcatus) Karsten
Stephanopyxis sp.
Synedra spp.
Thalassiosira antarctica Comber
T. gerlojji Ramirez
T. excentrica (Ehrenberg) Cleve
7". gracilis (Karsten) Hasle
T. gravida Cleve
7". lineata Zhuse
Landfast ice
Pack
ice
T. tumida (Janisch) Hasle
T. ritscherii (Hustedt) M. Peragallo
Thalassiolhnx longissima Cleve and Grunow
Trachyneis aspera M. Peragallo
Tropidoneis antarctica (Grunow) Cleve
T. belgicae (Van Heurck) Heiden
T. fusiformis Manguin
T. gaussti Heiden and Kolbe
T. glacialis Heiden and Kolbe
T. vanheurckii (Grunow) Cleve
+
+
+
+
+
+
+
Landfast ice
+
+
+
+
+
+
+
Autotrophic nanoflagellates
>
Chlorophytes
Chlamydomonas sp.
Prasinophytes
Mantoniella antarctica Marchant
Mantoniella squamata (Manton and Parke) Desikachary
Pyramimonas gelidicola McFadden el al.
Prymnesiophytes
Chrysochromuhna sp.
Phaeocystis pouchetit (Hariot) Langerheim
Z
>
+
+
+
+
m
W
O
+
+
Chrysophytes
Distephanus speculum (Ehrenberg) Haeckel
Paraphysomonas impforata Lucas
P. antarctica Takahashi
P. butcheri Pennick and Clarke
P. oligocycla Takahashi
P. vestita Takahashi
n
+
+
+
+
+
Parmales
Archaeomonads
Archaeomonas aerolata Deflandre
Litheusphaerella spectabilis Deflandre
+
+
NO
oo
TABLE 2.
Pack
ice
Pack
ice
Landfast ice
Cryptophytes
Autotrophic dinoflagellates
Prorocentrum sp.
+
+
Heterotrophic flagellates
Choanoflagellates
Acanthoeca brei'ipoda Ellis, 1929
Acanthoeorbis unguiculata Thomsen, 1973
Bicosta antenmgera Moestrup, 1979
Bicosta spinifera (Throndsen, 1970)
Calliacantha simplex Manton and Oates, 1979
Cosmoeca ventrkosa Thomsen, 1984
Crinolina aperta Leadbeater, 1975
Diaphanoeca grandis Ellis, 1929
Diaphanoeca multiannulata Buck, 1981
Diaphanoeca pedicellata Leadbeater, 1972
Kakoeca antarctka nom. prov.
Pan'icorbkula quadncostata Throndsen, 1970
P. socialis (Meunier) DeFlandre, 1960
Saepicula leadbeateri Takahashi, 1981
Savillea parva Ellis, 1929
Stephanoeca diplocostata v. pauckostata Throndsen, 1969
Bodonids
Bodo sp.
Rhynchomonas sp.
Euglenoids
Anisonema sp.
Petralomonas sp.
lncerta sedis
Cryothecomonas armigera nom. prov.
Landfast ice
Heterotrophic dinoflagellates
Cryptomonas cryophila Taylor and Lee
Gymnodinium spp.
t\
Continued.
Amphidmium hadai Balech, 1975
Amphidinium spp.
Gymnodinium spp.
Gyrodinium lachryma Meunier, 1907
Gyrodinium spp.
Protoperidinium spp.
Ciliates
+
+
+
+
-4+
+
+
+
+
+
+
+
+
+
+
+
+
+
Amphileptus sp.
Aspidisca antarctia Corliss and Snyder, 1986
Chilodonella pseudochilodon Deroux, 1970
Chlamydonella sp.
Codonellopsis gausii (Laackmann, 1909)
Cohnilembus grassei Corliss and Snyder, 1986
Condylostoma sp.
Didinium sp.
D. balbainh v. nanum Kahl, 1930
D. gartgantua Kahl, 1933
Euplotes antarctica Fenchel and Lee, 1972
Euplotes sp.
Holostkha sp.
Lacrymaria spp.
L. spiralis Corliss and Snyder, 1986
Myrionecta rubrum Grain el at, 1982
Pleuronema glaciale Corliss and Snyder, 1986
Salpingella spp.
Scuhcoahate spp.
Spiroprorodon spp.
S. piroprorodon garnsoni Corliss and Snyder, 1986
S. glaaalis Fenchel and Lee, 1972
Strobilidium spp.?
Strombidium spp.
Strombilidium rhyticollare Corliss and Snyder, 1986
Tachysoma parvulum Corliss and Snyder, 1986
Tontonia sp.
<
3
r
O
2
c/
o
TABLE 2. Continued.
Pack
ice
Trochilia sp.
Uronema sp.
Uronychia sp.
U. transtuga
Sarcodines
Unidentified amoebae
Unidentified hehozoans
Acanthocyptis sp.
Pinaciophora fluvialilis Greff, 1875
Neogloboqxiadrina pachyderma (Ehrenberg) (Globigerina
pachydertna)
Metazoa
Polychaetes
Harmothoe sp.
Pionosyllis sp.
Amphipods
Bovallia walherii
Cheirimedon femoratus
Eusirus antarcticus
Lepidopercrum cingulatum
Paramoera walkeri
Pontogeneia antarctica
Orchomenella sp.
Orchonicnopsis sp.
Landfast ice
Pack
Landfast ice
Cqpepods
Calanus propinquus
C. acutus
Ctenocalanus vanus
Dactylopodia sp.
Dissostichus mawsont
Drescheriella glacialis
Harpahcus sp.
Microcalanus pygmaeus
Oithona similts
Oncaea curvata
Paralabidocera antarctica
Rhincalanus gigas
Stephos longipes
Tisbe racovitzea
T. furcata
calanoid naupliar larvae
7
n
n
i—
n
M
Euphausiids
Euphausia superba Dana
E. crystallorphias
Thysanoessa macrura
W
0
>
Fishes
Pagothena borchgrevinki (Trematonnus borchgrevinki)
T. newnesii
* Sources: Aarset (1987); Ackley et al. (1978); Andriashev (1968); Corliss and Snyder (1986); Daly and Macaulay (1988); Fenchel and Lee (1972); Foster
(1987); Garrison and Buck (1985, 1989a); Garrison et al. (1987); Grossi (1985); Grossi and Sullivan (1985); Gruzov et al. (1967); Homer (1985rf); Hosiai and
Tanimura (1981, 1986); Krebs (1983); Krebs el al. (1987); Marchant et al. (1989); McConville and Wetherbee (1983); Mitchell and Silver (1982); Takahashi
et al. (1986); Takahashi (1981, 1987); Tanimura et al. (1984, 1988); Watanabe (1982, 1988). (+) present; (?) uncertain.
N
26
DAVID L. GARRISON
1984). A study by Palmisano and Sullivan
(1982), however, indicated that some species undergo physiological changes that
promote winter survival, so that resting cells
(i.e., dormant or resistant stages that are
not morphologically distinct) may, in fact,
be prevalent in ice.
A species list compiled from recent studies (see Table 2) shows the considerable
overlap between diatom species found in
land-fast and pack ice. In spite of the occurrence of some widely-distributed species,
it appears that there are some more-or-less
distinct assemblages (see Table 1). For
example, Grossi (1985) denned a diatom
assemblage associated with congelation ice
at McMurdo Sound. She also reported that
the composition of this assemblage was
influenced by the presence or absence of
an underlying platelet layer. Grossi and
Sullivan (1985) related the vertical distribution patterns in congelation ice to successive blooms in the ice and the differential
growth
of species
along
physiochemical gradients. McConville and
Wetherbee (1983) and Watanabe (1988)
have also described an under-ice mat, or
strand-like, diatom assemblage in land-fast
ice (see Table 1). The assemblages in fast
ice may reflect the incorporation of benthic or tychopelagic forms in these shallowwater environments. On the other hand,
diatom assemblages in the pack ice appear
to be derived largely from planktonic populations, which are concentrated in the ice
during its formation (Garrison et al., 1983).
The striking similarity between pack ice
and planktonic diatom assemblages has
tended to support the hypothesis that algae
released from melting ice floes provide an
important inoculum for planktonic populations in the pack ice region (Krebs, 1983;
Garrison and Buck, 1985; Garrison et al,
1987).
A variety of small (nano) and large
(micro) autotrophic flagellates occur in the
ice and may sometimes predominate over
the diatoms (Garrison and Buck, 1989a).
The relatively short list of flagellate species
(see Table 2) indicates that many nanoplankton cannot be readily identified by
light microscopy, and so far, relatively few
studies have utilized electron microscopy
to examine the ice-associated forms. Moreover, the nano- and microflagellates, as well
as other delicate forms may have been
missed in many studies because they can
easily be destroyed during the melting of
ice samples (Garrison and Buck, 1986).
The well known prymnesiophyte, Phaeocystis pouchetii occurs regularly in pack ice,
where it forms dense population cells
reaching up to 5 x 10' cells liter"1. Both
the solitary, motile cells and gelatinous colony lifestages are found in the ice. Phaeocystis is another planktonic species that
appears to be seeded from ice floes (e.g.,
Bunt, 1968; Garrison et al, 1987; Fryxell
and Kendrick, 1988). Other nanoflagellates have resting stages in ice. Cyst-like
stages that Deflandre (Deflandre and
Deflandre-Rigaud, 1970; Mitchell and Silver, 1982) called archaeomonads are very
abundant in ice floes. We have found
archaeomonads in pack ice floes at densities of 10 4 -10 7 liter" 1 , and Takahashi etal.
(1986) reported similar forms in land-fast
ice. We assume that archaeomonads are
resting stages of chrysophytes present in
ice, but have been unsuccessful in germinating them to verify their affinities. Takahashi (1987), however, has identified both
siliceous cysts and the vegetative stages of
the chrysophyte Paraphysomonas in land-fast
ice.
Autotrophic dinoflagellates belonging to
the so-called unarmoured genera Gymnodinium, Gyrodinium, and Amphidinium are
sometimes abundant in the ice. In some
samples we have found a thick walled spiny
cyst, which has now been identified as a
hypnozygote of an autotrophic form (Buck
etal, 1989).
Whereas most studies of ice communities
have included estimates of algal abundance
(see Homer, 1985c), only in recent studies
has there been an attempt to quantify heterotrophic members of the ice microbial
community. Sullivan and co-workers (e.g.,
Sullivan and Palmisano, 1984; Sullivan,
1985; Kottmeier and Sullivan, 1987) have
shown that bacteria are abundant in both
land-fast and pack ice. We have found that
heterotrophic flagellates and ciliates also
comprise a significant fraction of the heterotrophic biomass in pack ice (Garrison et
ANTARCTIC ICE BIOTA
al, 1986; Garrison and Buck, 1989a).
Whether flagellates and ciliates are as prevalent in land-fast ice assemblages as in the
pack ice is uncertain (see Grossi etai, 1987;
Kottmeier et al., 1987).
The heterotrophic flagellates in pack ice
include bodonids, choanoflagellates,
euglenoids, and dinoflagellates (see Table
2). Many of the small forms are nondescript and can be recognized as heterotrophic nanoflagellates only when examined
by using epifluorescence microscopy.
Choanoflagellates, however, have distinctive loricas and can be readily identified.
Although there is no quantitative information about the abundance of heterotrophic nanoflagellates from fast ice, Takahashi (1981) has found some of the same
choanoflagellate species in fast ice that
occur in the pack ice. The heterotrophic
nanoflagellates are phagotrophs and feed
primarily on bacteria, although Marchant
(1985) has reported that choanoflagellates
may also ingest small autotrophs and detritus. One of the most common of the larger
phagotrophic flagellates resembles a chlorophyte in its external appearance, but
preliminary studies by transmission electron microscopy have indicated that it is
probably not a chlorophyte (Thomsen et
al., unpublished observations).
The largest heterotrophic flagellates in
ice are the dinoflagellates. The heterotrophic forms (e.g., Gyrodinium and Amphidinium) closely resemble the autotrophic forms,
and we have found that it is necessary to
use fluorescence microscopy to determine
their primary trophic role. One of the largest, and as yet unidentified, heterotrophic
dinoflagellates leaves little doubt about its
nutritional source because it usually contains food vacuoles filled with large diatoms, which occupy much of the body volume (Buck etal., 1990).
The ciliated protozoa are also well represented in pack ice communities; and at
times, they comprise a major fraction of
the heterotrophic biomass (Garrison and
Buck, 1989a). The ciliates associated with
Antarctic ice communities were known only
from a brief report by Fenchel and Lee
(1972) until Corliss and Snyder (1986)
examined samples we collected from ice
27
during the austral spring of 1983. They
found 26 separate taxa with 7 species which
were previously undescribed, suggesting
the diversity that is likely to be uncovered
with more extensive systematic studies.
The most abundant ciliates in pack ice
floes are the non-sheathed oligotrichs (e.g.,
Strombidium spp.), which are similar to the
forms that are common in planktonic
assemblages (Garrison and Buck, 19896).
The well-known symbiont-bearing ciliate,
Myrionecta rubrum (Mesodinium rubrum; see
Taylor, 1982), is also frequently found in
ice at densities up to 105 cells liter" 1 (Garrison and Buck, 1989a). Spindler (1988)
also reported ciliates throughout the ice in
the southeastern Weddell Sea but at densities considerably lower (e.g., usually < 102
liter"1) than we have found in other locations in pack ice (Garrison and Buck,
1989a). Grossi etal. (1987) and Kottmeier
et al. (1987) reported that ciliates are present in fast ice communities at McMurdo
Sound but gave no indication of the species
or their abundances. Many specimens
examined by Corliss and Snyder (1986) and
in the course of our studies were found to
contain ingested diatoms and dinoflagellates. Other ciliate species from ice consume bacteria and some of the larger species (e.g., Didinium) are known to be
predators on other protozoa.
A variety of other protozoa including
amoeba, heliozoans, and foraminiferans are
also found in ice (see Table 2; Garrison and
Buck, 1988, 1990). Foraminiferans are
large (100-200 /an) but their densities are
low (maximum 5 x 102 liter"'; Lipps and
Krebs, 1974; Spindler and Dieckmann,
1986; Garrison and Buck, 1989a), so their
contribution to biomass is low relative to
the ciliates and heterotrophic flagellates.
Foraminiferan abundances in ice, which
exceed densities in the underlying water
column by an order of magnitude, may be
the result of harvesting and concentration
during frazil ice formation, as has been
suggested for other ice-associated biota
(e.g., Garrison et al., 1983; Spindler and
Dieckmann, 1986).
Metazoa associated with Antarctic sea ice
include organisms actually living in sea ice
as well as those on the undersides of floes
28
DAVID L. GARRISON
and in the underlying water (see Table 2). may reach the underlying benthos. Dayton
Many of the amphipods associated with fast and Oliver (1977) have documented the
ice are benthic species that seasonally col- density and richness of the benthic comonize the undersides of ice floes from the munity at McMurdo Sound. Sullivan et al.
adjacent benthos (Rakusa-Suszczewski, (1985) have argued that much of the pro1972; Richardson and Whitaker, 1979; duction in this region must be associated
Sagar, 1980). A variety of copepods have with the sea ice.
also been associated with ice, but for most,
The food web relationships in the pack
their relationship with the ice is not well- ice regions are becoming increasingly wellknown (e.g., Hoshiai and Tanimura, 1986; known, but the quantitative importance of
Foster, 1987; Martin, 1988). However,. the ice-associated food web in this system
Dahms and Dieckmann (1987) reported is still unclear. Garrison et al. (1986) and
that the harpacticoid Drescheriella glacialis Garrison and Buck (1989a) have shown that
reproduces and develops in the ice, and heterotrophic flagellates and ciliates are
Tanimura et al. (1988) have found that the abundant in pack ice floes. A conceptual
nauplii and first three copepodite stages of food web, based on examining trophic staParalabidocera antarctica may live within the tus and prey consumed by nano- and
ice. Three species of euphausiids are also microheterotrophs, indicates that there is
commonly associated with ice and are a complex food web in ice with energy passbelieved to comprise the most important ing through one or two steps before reachlarge pelagic consumers of the ice biota ing micro sized organisms (Fig. 2). In some
(O'Brien, 1987; Daly and Macaulay, 1988; samples, a substantial amount of the algal
Marschall, 1988; Daly, 1990).
and bacterial production would be required
to support the biomass of heterotrophic
members of the ice community (Garrison
Food webs
Andriashev (1968) was the first to out- et al, 1986; Garrison and Buck, 1989a;
line a conceptual food web associated with unpublished data). The biomasses of both
the ice biota in nearshore, fast ice regions. the autotrophs and heterotrophs in the ice
Andriashev recognized that there was a are usually 1-2 orders of magnitude greater
"true" ice fauna as well as organisms in the ice than in the underlying water colaggregating below ice and apparently feed- umn (Garrison and Buck, 1989a). One
ing on the ice biota. Several studies in the explanation for the abundance of the nanonearshore, fast ice regions have confirmed and microconsumers is that the ice proAndriashev's speculations, and recent vides a suitable growth environment for
studies in the pack ice suggest that a sim- prey items (i.e., algae and bacteria) while
ilarly organized food web, but comprising providing a refuge for the heterotrophic
different species, also occurs in these protozoa. Although larger consumers such
regions. So far, only the qualitative food as amphipods, copepods, and euphausiids
web relationships have been established, may at times be found within the ice, seaand the amount of energy passing through sonal weathering of the ice or other deformational processes may be required to
ice-based food webs is speculative.
expose the ice microbial community to
In the fast ice regions, benthic amphi- these consumers (Meguro, 1962; Tanipods are the conspicuous large consumers mura et al, 1984; Marschall, 1988).
of the ice biota (e.g., Richardson and Whitaker, 1979). Copepods within and under
A considerable amount of attention is
ice floes also consume the ice microbiota now being given to the association of the
(Tanimura et al., 1984; Hoshiai and Tani- Antarctic krill, Euphausia superba, with the
mura, 1986; Hoshiai <?* al., 1987). Hoshiai sea ice community. There are a number of
and Tanimura (1981) have reported that reports documenting that E. superba is frethese copepods are included in the diet of quently found on the undersides of pack
the young of the nototheniid fish, Trema- ice floes (O'Brien, 1987; Daly and Macautomus borchgrevinki. In the shallow water lay, 1988; Marschall, 1988; Daly, 1990).
regions, much of the ice-based production Both laboratory (Hamnerrf al., 1983; Mar-
29
ANTARCTIC ICE BIOTA
•
•
'
•
*
Euph«u»l«
super ba
FIG. 2. A conceptual food web for the pack ice microbial community. A.F., autotrophic flagellates; H.F.,
heterotrophic flagellates; A. Dino, autotrophic dinoflagellates; H. Dino, heterotrophic dinoflagellates; Bact,
bacteria; DOM, dissolved organic material; Met., small metazoans. Solid lines show feeding relationships that
have been documented. Dashed lines show predator-prey relationships that are known in other systems but
have not been confirmed in sea ice. None of the feeding rates are known. Figure from Garrison et al. (1986)
with permission from BioScience.
schall, 1988) and field observations
(O'Brien, 1987; Stretch et al., 1988; Marschall, 1989a; Daly, 1990) indicate that krill
are able to seek out and feed on the microbial biomass in ice communities. If production in the ice proves to be an important seasonal resource for Euphausia superba
then the importance of the ice biota to the
Antarctic food web will need to be re-evaluated.
Role and importance of the ice biota
There is some uncertainty in comparing
species assemblages among the various ice
habitats because these data have been gathered by different workers using different
methodology and often focusing on
selected groups of the ice-associated biota.
The evidence for differences between
nearshore fast ice and drifting pack ice,
however, includes differing environmental
regimes and a differing structural composition of ice as well as a different structure
of the biotic assemblage. If community
dynamics differ in these two habitats, it is
unlikely that the information gathered
from studies of nearshore fast ice will be
suitable for understanding biological processes in the more extensive pack ice
regions. Until there are better estimates of
productivity in sea ice communities, particularly in the pack ice regions, their
importance in the Antarctic marine food
web will remain uncertain. The abundance
of heterotrophs in some ice assemblages
suggests that a considerable amount of the
ice-based production could be consumed
in situ. The consumption rates of the ice
fauna, however, are unknown. Studies of
community level processes in both the fast
30
DAVID L. GARRISON
and pack ice environments are relatively
recent, and a considerable amount of work
needs to be done to determine the functional relationships among various organisms associated with ice. Because ice is an
ephemeral habitat, ice-associated material
will eventually be released into the water
column, where it should have some impact
on the pelagic community. As ice floes melt
and deteriorate, accumulated microbial
biomass, fecal material and other detritus
will become available to pelagic consumers, and the living organisms released from
ice may provide an important "seed stock"
to developing planktonic populations (e.g.,
Garrison et al., 1987).
ACKNOWLEDGMENTS
This study was supported by NSF
grants to D. L. Garrison and M. W. Silver (DPP8218747), D. L. Garrison
(DPP8420184) and to the Smithsonian
Sorting Center (DPP8214878). I thank
John Corliss and Richard Snyder for their
systemic work on ciliates. As indicated by
citations in the text, the ice community
studies have been conducted with the assistance of Kurt Buck, and 1 thank him for
his help in preparing this review. I have
made extensive use of materials summarized in Sea Ice Biota, and I am indebted to
Rita Horner for her efforts to produce this
excellent, comprehensive volume. Several
reviewers including M. Boysen, K. R. Buck,
R. Horner, Karin Lange, O. Lonne and K.
Watanabe provided comments, suggestions and corrections at various stages in
the development of this manuscript. Maureen Leimbach typed the manuscript and
patiently made the corrections on the final
revisions.
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