Ecology of bottom ice algae: I. Environmental controls and variability

Journal of Marine Systems, 2 (1991) 257-277

257

Elsevier Science Publishers B.V., Amsterdam

Ecology of bottom ice algae: I. Environmental controls and variability G . F . C o t a a, L. L e g e n d r e

b M.

Gosselin b and R.G. Ingram c

a Graduate Program in Ecology, Unioersity of Tennessee, Knoxville, TN 37996-1610, USA b DOpartemant de biologic, Unioersit~ Laoal, Quebec, Que. G1K 7P4, Canada " Meteorology Department, McGill Unioersity, Montreal, Que. H3A 2K6, Canada

Received September 9, 1990; revised version accepted February 11, 1991

ABSTRACT Cota, G.F., Legendre, L., Gosselin, M. and Ingram, R.G., 1991. Ecology of bottom ice algae: I. Environmental controls and variability. J. Mar. Syst., 2: 257-277. Over large ocean areas of the Arctic, Subarctic and Antarctic, which are covered by landfast sea ice during springtime, high concentrations of microalgae have been observed in the interstices of the lower margin of sea ice floes and, in some cases, in a thin layer of surface water immediately under the ice cover or associated with semi-consolidated frazil ice. Ice algal blooms enhance and extend biological production in polar waters by at least 1-3 months. Biomass accumulation of sea ice algal populations ultimately depends upon the duration of the growth season, which is largely a function of climatic and environmental variability. Growth seasons are shorter at lower latitudes because of abbreviated photoperiods, warmer air temperatures and earlier ablation and break up. Environmental factors, which regulate ice algal distributions and dynamics, display characteristic scales of time/space variance. Sea ice habitats are much more stable than planktonic environments, because ice is not subject to large vertical displacements in the irradiance field. Temperature and salinity are relatively constant over most of the growth period. However, nutrients must be supplied to relatively thin, dense layers of cells and fluxes are variable depending on ice growth and hydrodynamics. Although the occurrence of prolonged blooms of ice algae at the ice-water interface is a widespread phenomenon, there are important differences between the growth habits and environments of several well-studied sites. Recent observations from seasonal studies of these sites are compared and contrasted with an emphasis on how the dominant scales of environmental variability influence ice algal populations.

Introduction

descriptions a n d terminology. W e refer the reader to reviews by Weeks a n d Ackley (1982), H o r n e r

Sea ice takes o n m a n y shapes or forms, d e p e n d ing u p o n its history. However, these n u m e r o u s types can be segregated into two basic categories, frazil a n d congelation, based o n their m e c h a n i s m of f o r m a t i o n a n d crystalline structure. Initially,

(1985a), M a y k u t (1985), G a r r i s o n et al. (1986), P a r k i n s o n et al. (1987) a n d H o r n e r et al. (1988) for general discussions of related interest a n d relev a n t bibliographies. I n d i v i d u a l , u n c o n s o l i d a t e d

sea ice is formed from frazil ice, which results from supercooled seawater. P r o d u c t i o n of frazil ice is most c o m m o n in leads or p o l y n y a s a n d near ice edges a n d glacial ice shelves (Weeks a n d Ackley, 1982; Barry, 1988). A l t h o u g h frazil ice is defined specifically in the physical literature, it occurs in several forms with v a r y i n g degrees of c o n s o l i d a t i o n a n d some c o n f u s i o n has arisen i n 0924-7963/91/$03.50

© 1991 - Elsevier Science Publishers B.V.

frazil ice crystals ( n u c l e a t i o n spheroids a n d discoid or stellate crystals) exist below or near the sea surface. S e m i - c o n s o l i d a t e d forms of frazil ice include "grease", " s l u s h " , " n i l a s " or " p a n c a k e " ice o n the sea surface a n d " u n d e r w a t e r " ( " u n d e r - i c e platelet") frazil ice in various formations. All rights reserved Frazil ice crystals m a y also b e c o m e consolidated i n t o ice floes at a n y level in the ice c o l u m n , p a r t i c u l a r l y the u p p e r surface. C o n s o l i d a -

258

tion is initiated when concentrations of frazil ice crystals exceed 40% by volume and the agglomerated ice begins the transition to a more solid phase with distinct mechanical properties (see Weeks and Ackley, 1982). Congelation ice exists as consolidated sheets of predominantly columnar ice with a particular crystal orientation which results from accretion at the lower margin; it includes various kinds of first-year (e.g. "young", "gray", "gray-white" or "annual") ice and multiyear ( > second-year) ice floes. Sea ice is further classified as landfast (attached to shore) or pack (drifting) ice. The structural characteristics of ice floes depend on events during formation and growth. Floes thicken by accumulating more frazil ice from the water column (and subsequent crystal growth) a n d / o r by the addition of congelation ice at the lower margin. Ice floes are usually a mixture of these two basic ice types, but frazil ice crystals usually comprise only a small percentage of ice columns (i.e. above the surface transition zone) except in regions where supercooling is common (Weeks and Ackley, 1982). After the initial freezeup, frazil ice tends to be relatively scarce in the Arctic compared to the Antarctic (Maykut, 1985) and is prevalent only in particular areas with significant open water such as Weddell Sea ice edges or near floating glaciers like the Ross Ice Shelf in McMurdo Sound. Due to its inaccessibility, observations on pack ice are very limited in space and time, but indicate that pack ice environments can be extremely variable and complex with numerous habitats (e.g. Weeks and Ackley, 1982; Garrison et al., 1986). Ice structure is very much dependent upon environmental conditions, especially temperature and, consequently, sea ice evolves seasonally with characteristic changes in thickness, density, salinity, porosity, brine volume, etc. Changes in ice structure are fundamental to ice algal colonization, determining habitat availability and variability. For example, in early spring when landfast congelation ice is still accreting there is an almost linear temperature profile (e.g. from - 30°C in air to - 1 . 8 ° C in water) across the ice sheet and the ice above the skeletal layer is very hard and cold. During this period, visible pigmentation, indica-

COTA ET AL.

tive of substantial biomass accumulation, is usually restricted to the lowest few centimeters, which are relatively soft (it can be scraped off with a knife; bite a fresh ice cube versus an older, partially melted one to appreciate the difference) and warm (slightly below surface seawater temperature which is at its freezing point). It appears that the lower interface of landfast congelation ice is the most suitable habitat available until later in the year when the ice sheet warms up and becomes more porous. Pack ice differs in that more surfaces, which are bathed by water, are available along the sides and relatively porous interior (Garrison et al., 1986). As the season progresses much of the fast ice starts to melt and breaks up into smaller floes; it becomes detached from the shore and intermingles with pack ice. Because sea ice and its habitats are so varied, they should be described in detail and compared with caution.

Ice algal assemblages Marine microalgae are associated with a variety of ice types, ranging from frazil ice, to annual or multi-year sea ice floes and even the margins of freshwater icebergs (Whitaker, 1977; Homer, 1985a; Garrison et al., 1986; H o m e r et al., 1988). Algae are also found in or on sea ice throughout the year, but cells are not necessarily actively growing and some habitats may be suitable only under certain conditions (Fig. 1). We utilize the basic nomenclature of H o m e r et al. (1988) to describe sea ice environments and units for quantitative reporting on ice algal assemblages. Surface, interior and bottom are primary descriptors of the location of the assemblage on/within the ice sheet at the time of sampling. Additional modifiers, including infiltration, pool, brine channel, band, interstitial and sub-ice, were suggested to distinguish between habitats of particular assemblages. However, in some cases further elaboration and modification such as "attached" or "unattached" may be required to distinguish between taxonomically, temporally, spatially a n d / o r functionally distinct groups which might otherwise mistakenly be lumped into the same ice

ECOLOGY OF BOTTOM ICE ALGAE, I

259

lution of observations on most sea ice systems makes it difficult to ascertain interrelationships or to discriminate between possible alternate descriptions and interpretations. More comprehensive, high-resolution, time-series observations are critical to improve our understanding of the structure and function of sea ice ecosystems. There are also at least two other "attached" sub-ice assemblages which have a common characteristic "strand" structure but differ floristically, temporally or spatially. Apollonio (1985) summarized observations on a summer "sub-ice strand" assemblage dominated by Melosira spp., a centric diatom; strands or amorphous masses of mucilaginous slime are fairly common on or near pack ice in the Arctic in summer. During austral spring in the Antarctic, there are sub-ice strands of diatoms, most of which are tube-dwelling pennate forms, associated with hard congelation ice (McConville and Weatherbee, 1983) or with "subice frazil" assemblages (Grossi et al., 1987). Platelet (or under-ice platelets) ice is equivalent with semi-consolidated, underwater frazil ice where the crystals have become agglomerated and grown in size. The sub-ice frazil layer is an irregular honeycomb of ice crystals of assorted sizes which contains more seawater (usually > 80%) than ice. Frazil layer thickness can vary substantially over meter scales and significant turbulence (e.g. a diver's motions or bubbles) may disrupt the irregular lattice of frazil (platelet) ice matrix because the crystals are only loosely associated. We recommend "frazil assemblage" for all algae associated with frazil ice crystals ranging from unconsolidated grease ice composed of " y o u n g " frazil ice crystals (i.e. "surface frazil") to semi-consolidated "sub-ice frazil" (under-ice platelet) assemblages (e.g. see Garrison et al., 1986). As more information becomes available, further distinctions may be necessary to distinguish different ice algal assemblages. To avoid confusion it is imperative to provide an accurate and explicit description of the environment, organisms, methods and time frame of observations to facilitate intercomparisons of sea ice systems. Moreover, we caution that these terms do not necessarily describe the actual origin of the cells as suggested by Horner et al. (1988), because phyto-

t ASSEMBLAGES SURFACE

iLt ASSEMBLAGES INTERIOR

t ASSEMBLAGES BOTTOM S Fig. 1. Schematic description of sea ice and potential habitats for various types of ice algal assemblages (adapted from H o m e r et al., 1988). Three sub-ice assemblages are depicted. F r o m left to right they are the frazil, strand and unattached free-floating. See text for details.

algal assemblage. For example, there are several types of sub-ice assemblages such as "sub-ice frazil" and "sub-ice strand" which occur in particular locations or different seasons (see below).

Bottom and sub-ice assemblages A number of bottom and sub-ice assemblages appear to have different specific compositions, habitats, growth seasons a n d / o r physiological behaviors. In addition to an "attached" bottom interstitial assemblage, there is also a persistent, "unattached" (bottom) sub-ice assemblage found floating immediately below the ice-water interface in southeastern Hudson Bay which co-occur in the spring (see Legendre and Gosselin, 1991). By contrast, the "unattached" mats of (bottom) sub-ice algae described by Cross (1982) near an ice edge in late spring were probably "attached bottom interstitial" cells which had been released into the water recently; we have often observed similar floating mats of "sloughed" algae in Barrow Strait during late spring (Cota and Horne, 1989; Cota, unpubl.). Very limited temporal and spatial reso-

260

plankton cells scavenged by frazil crystals (e.g. Garrison et al., 1983; Demers et al., 1984) or hydraulically pumped (see Niedrauer and Martin, 1979; S.F. Ackley, pers. commun.) from the water column could be a source of contamination in any of these layers. There can be considerable overlap between assemblages in sea ice and the plankton (e.g. Horner, 1985b; Garrison et al., 1987), however one cannot distinguish between, import, export or in situ growth based on the occurrence of a species in either environment. The origins and fate of most ice algal assemblages are not well known and because of the complexity of these questions and the processes involved, they promise to remain enigmatic for some time to come.

Interior assemblages A few algal cells are usually scattered throughout ice floes at all seasons, but lacking time-series observations, it is rarely possible to determine the origin and in situ activity of cells. Their presence may reflect passive accumulation by physical processes rather than biological activity (Ackley et al., 1979). Bottom ice algal layers may be overgrown in fall when conditions for growth deteriorate, ice accretion may be more rapid than rates of migration or growth, or alternatively, phytoplankton may be scavenged from the water column (Garrison et al., 1983). Although these cells may retain their pigmentation and remain viable (Hoshiai, 1977; McConville and Wetherbee, 1983), there may not be net population growth in the ice. Pigment bands within the ice floes are relatively rare in landfast first-year ice, but are more common in multi-year ice at the interface between growth seasons. "Brine channel" assemblages with a mixture of ice algae and phytoplankton are most common after the onset of melt (McConville and Wetherbee, 1983). Unequivocal, direct evidence to substantiate the in situ activity and growth of interior populations is unavailable at present. Most reports of interior assemblages are from pack ice in the Antarctic (Garrison et al., 1986; H o m e r et al., 1988), but they may also occur in the Arctic during summer when the ice is warm and porous.

COTA ET AL.

Surface assemblages Surface assemblages are most common in the Antarctic. "Infiltration assemblages" occur primarily on pack ice with heavy snow cover which has been flooded with seawater at the snow-ice interface (Meguro et al., 1991). "Surface pool assemblages" form in melt ponds, tidal cracks and leads. Studies on interior and surface assemblages are comparatively rare and most observations are descriptive. Although they are much more extensive on an areal basis, inclusion of pack ice systems in our discussion seems premature. They have been undersampled even more than landfast ice, observations are largely descriptive and there are no published time-series observations. Subsequent discussion focuses on bottom or sub-ice assemblages which are known to grow in spring on or very near the lower interface of landfast sea ice. Boreal or austral spring are hereafter called spring. Because of large historic data bases and first-hand knowledge, we concentrate on three sites which have been studied intensively over the local vernal bloom.

Environmental comparison: arctic, subarctic and antarctic Northern Hemisphere data show variations over the annual cycle of monthly averaged sea ice extent range from a minimum of approximately 8.5.10 6 km 2 in September to a maximum of about 1 5 - 1 0 6 km 2 in March (Parkinson and Cavalieri, 1989). By comparison, the m i n i m u m / maximum sea ice extent in the Antarctic ranges from about 3.5 to 20-106 km 2 over the annual cycle (Zwally et al., 1983). The minimum value in both cases mainly represents multi-year ice. The area difference between maximum and minimum values are largely pack ice in the Antarctic versus landfast ice in the Arctic. Since the major contribution of sea ice algae is found under landfast ice, the large difference in the annual range of sea ice extent between the polar regions does not imply a similar contrast in algal productivity. Most of our discussion concerns landfast ice communities from four areas including Barrow

ECOLOGY OF BOTTOM ICE ALGAE, I

261

Strait (74°40'N) in the center of the Northwest Passage in the high Arctic, another high Arctic site on the Beaufort Sea shelf (70 o 20'N) offshore of the Mackenzie River, a subarctic site in southeastern Hudson Bay (55 o 30'N) and McMurdo Sound at about 77°45'S in the Antarctic. With the exception of the Beaufort Sea site, these areas have been studied intensively for at least 5 spring field seasons and thus have the largest published data bases available. The second and third sites are both impacted by rivers, the Mackenzie and Great Whale, respectively. Although the Mackenzie delta site has received the least attention (Pett et al., 1983), it may be more representative of large areas of the Arctic shelf where large freshwater inputs occur, particularly from the Soviet Union (Aagaard and Carmack, 1989). Other sites have also been studied intensively and some have large, multi-year data bases; some key citations (also see references cited therein) are given below. Similar seasonal studies on shorefast ice have been conducted in the high Arctic off Alaska in the Beaufort Sea (Homer and Schrader, 1982) and in the Chukchi Sea (Alexander et al., 1974; Clasby et al. 1976), in

subarctic Frobisher Bay (Hsiao, 1988; Grainger and Hsiao, 1990) and at several sites in the Antarctic (Hoshiai, 1977; McConville and Wetherbee, 1983). There are some important fundamental differences in the climatic and oceanographic conditions of these four areas (Table 1). The high latitude sites are well above the Arctic or Antarctic Circles and thus have more extreme climatic changes (e.g. solar radiation and air temperature) seasonally. During the winter-spring transition incident irradiance increases dramatically from continuous darkness to relatively high levels (ca. 1300-1600 ~E m -2 s -1 at solar noon on clear days which is similar to temperate regions) with continuous but variable daylight by mid-bloom. On the other hand, in Hudson Bay the daylength varies from 7.5 to 18.5 h over the entire year. Average air temperatures at the subarctic site range from about - 1 0 to +10°C during the bloom (April through mid-May) (Gosselin et al., 1985), but increases from - 3 0 to + 2°C over the spring bloom period at the high latitude sites (Cota et al., 1987; Cota and Sullivan, 1990). Ice thickness for

TABLE 1 Environmental conditions for ice algal study areas in the Subarctic, Arctic and Antarctic. Months are roman numerals. Irradiances are m aximu m surface incident at solar noon. Water temperature, salinity, nutrients and currents are near surface values Condition

SE Hudson Bay

Beaufort Sea

Barrow Strait

Mc Murdo Sound

Latitude

55'30'N

70°20'N

74°40'N

77°45 ' S

Bloom period

IV 1 - V 15

III 1 5 - V I 15

III 1 5 - V I 15

X 1 - X I I 31

Air temperature (° C)

- 10 to + 10

- 30 to + 2

- 30 to + 2

- 30 to + 2

Day - length (h)

15-18

16-24

16-24

16-24

Ice thickness (m)

1.0-1.2

1.4-1.9

1.4-1.9

1.8-2.2

Snow depth (cm)

0-40

0-40

0-40

0-40

Water temperature (o C)

- 1.4 to 0.05

- 1.7 to - 1.8

- 1.7 to - 1.8

- 1.8 to - 1.9

Maximum irradiance 700-1600

700-1400

700-1400

800-1600

Salinity, sfc. (ppt)

(I 0, #E m -2 s -1 )

4-28

12-33

32-33

34-35

Sal. grad (0 -5 0 m)

4-30

2-11

< 0.2

< 0.1

Nitrate (uM) Silicic acid (/~M)

0.2-3.3 1-30

6-9 25-58

2-10 4-32

25-35 65-75

Phosphate (# M) Max. currents (cm s - l)

0-1 5-10

0.2-1.2 5-10

0.5-2.3 45-60

1.2-2.5 15-20

Tidal range (m)

0.2-1.5

0.1-0.4

0.4-1.6

0.1-1.0

Storm frequency (d) Max. biomass

5-6

3-5

4-6

3-6

10-30

10-120

100-300

150-300

(mg Chl m -

2)

262

unrafted annual (first-year) ice is around 1-1.2 m in the Subarctic versus 1.4-2.3 m at high latitude. The range of snow covers are similar at all of these sites, but mean snow depth in the high Canadian Arctic averages around 10 cm, varying from about 2 to 40 cm (Cota, 1985; Cota and Horne, 1989; Welch and Bergmann, 1989). Snow cover in McMurdo Sound tends to be less than 25 cm on average (C.W. Sullivan, pers. commun.) and in southeast Hudson Bay snow cover is typically between 15-40 cm during April (Gosselin et al., 1986, 1990). Most of the snow in southeast Hudson Bay melts by late April and seasonal variation in transmitted irradiance is dominated by changes in snow cover (Gosselin et al., 1985, 1990), unlike the high latitude sites, where solar flux increases seasonally but the snow cover is relatively constant up until the melt in late spring (Maykut, 1985; Cota and Horne, 1989). The sea ice system in McMurdo Sound is somewhat unique because it is often composed of two separate layers, the congelation ice sheet and the semi-consolidated frazil (platelet) ice, with a very different structure (SooHoo et al., 1987; Barry, 1988). The extent and thickness of the frazil ice layer in McMurdo Sound varies temporally and spatially (Garrison et al., 1986; Grossi et al., 1987; Barry, 1988). The interface between the two ice types intergrades to some extent and large crystals of frazil ice, which often have high levels of biomass (e.g. Grossi et al., 1987), may be partially attached to the congelation ice, contaminating congelation ice samples (Cota and Sullivan, 1990). Frazil ice layers are entirely absent in most other locations (e.g. McConville and Wetherbee, 1983; Maykut, 1985). However, if present, a layer of frazil ice should act as a baffle, damping currents and increasing the thickness of the viscous sublayer near the boundary. In November, during the middle of the spring bloom, current velocities in McMurdo Sound are typically less than 15 cm s - l ; periodic flows are dominated by tidal components at diurnal and fortnightly frequencies in month-long records (Lewis and Perkin, 1985; Mitchell and Bye, 1985; Barry and Dayton 1988). Additional non-tidal forcing of currents in McMurdo Sound is probably dominated by events such as atmospheric

COTA ET AL.

pressure changes due to the passage of weather systems at 3-6 day intervals (Cota and Sullivan, 1990), but longer data records are needed such as those from western Hudson Bay (Prinsenberg, 1987). In spring tidal forcing in Barrow Strait dominates local currents with speeds up to 45-60 cm s-1, but residual mean geostrophic flows reach speeds of 10-15 cm s -1 (Cota et al., 1987; Prinsenberg and Bennett, 1987). In southeast Hudson Bay the current regime is much less energetic. However, variability of the flow adjacent to the underside of the ice has an important effect on algal productivity (Gosselin et al., 1985; Rochet et al., 1986; Demers et al., 1989; Ingram et al., 1989). Ingram and Larouche (1987) found the tidal and the non-tidal low frequency current signals to be of similar magnitude. Maximum near-surface values were typically < 10 cm s -1 offshore of the Great Whale River plume. Shirasawa and Ingram (1991) have described the 3-D turbulent velocity regime under the ice-water interface and its dependence on extemal forcing and local stratification. Lepage and Ingram (1991) show the marked attenuation of both the tidal and long period current regime by the ice cover. They also describe the very stable stratification in the upper water column that occurs following initiation of ice melt but prior to breakup of the landfast ice sheet into pack-ice floes. This limits upward nutrient flux to the interface as well as providing a brackish environment. Few spring observations are available for the Mackenzie shelf area of southern Beaufort Sea. The upper layer current regime is similar in magnitude to that of SE Hudson Bay (Aagaard, 1984). Maximum tidal range at Herschel Island is the smallest of the four sites considered. The range of temperature and salinity values, as well as vertical stratification in the upper water column in the southern Beaufort Sea and southeast Hudson Bay are similar and contrast markedly with conditions in Barrow Strait and McMurdo Sound. Long-term, fairly high resolution data records have proved useful in identifying the dominant scales of forcing and variability in local currents, which may, in turn, be very important to biological activities (Gosselin et al., 1985; Cota et al., 1987). For example, using year-long current records from western Hudson Bay, Prinsenberg

263

ECOLOGY OF BOTTOM ICE ALGAE, I

(1987) partitioned current energy to illustrate the impact of a sea ice cover on tidal, meteorological and seasonal density-driven circulation. During winter-spring (mid-February to mid-May), when Hudson Bay is completely covered (almost tentenths, see Parkinson et al., 1987; Parkinson and Cavalieri, 1989) with landfast ice, tidal components again dominated currents with speeds up to 30 cm s -~. Attenuation and phase shift of the tidal signal caused by the ice is discussed in Prinsenberg and Ingram (1991). Long period non-tidal components were closely related to the passage of weather systems which had a periodicity of 4 - 6 days, similar to that found by Ingram and Larouche (1987). Inertial periodicity caused by short-term wind forcing was greatly reduced under the ice cover (Prinsenberg and Ingram, 1991).

Variability of important environmental factors Given that temperature and salinity are relatively constant during bloom periods, the two most important environmental factors, which are potentially limiting, are irradiance and nutrients (Gosselin et al., 1985, 1990; Cota et al., 1987, 1990; Grossi et al., 1987; Michel et al., 1988; Smith et al., 1988; Cota and Sullivan, 1990). Irradiance and nutrient fluxes appear to influence, if not control, biomass accumulation, biochemical composition and the physiological response(s) of the ice algae in the systems examined to date. Similar to the situation in the plankton, these resources have respective sources above and below the populations. However, ice algal layers are highly compressed and, despite their small vertical scale, are often highly stratified in the vertical (Smith et al., 1990; Cota and Smith, 1991). Most irradiance incident at the snow surface is reflected because of high albedo (Maykut, 1985) and light which finally reaches cells within the ice algal layer must pass through overlying snow, ice and algae (SooHoo et al., 1987; Smith et al., 1988). Nutrients adequate to account for the observed biomass accumulations must be supplied primarily from the water column (Gosselin et al., 1985; Cota et al., 1987, 1990; Demers et al., 1989; Cota and Sullivan, 1990).

Irradiance and nutrient availability change over the course of a bloom, since both are subject to natural variability and to density-dependent effects. At the beginning of the vernal growth season, irradiance is in fact the sole factor that limits the ice algae, since biomass is then relatively low and nutrients are abundant relative to algal requirements (Smith et al., 1988; Cota and Home, 1989; Gosselin et al., 1990). As the season progresses the ice algae must optimize their growth rates to the ambient light and nutrient regimes which have different but overlapping scales of temporal variability. Incident irradiance varies primarily seasonally (weeks-months), over diel cycles (hours-day) and with cloud cover (minutes-days). Nutrient fluxes are closely related to ice growth and currents which reflect the dominant local physical forcing and span scales of hours to weeks (Gosselin et al., 1985; Cota et al., 1987; Ingram et al., 1989). Light and nutrient limitation may be influential sequentially as the season progresses (e.g. Cota et al., 1987; Gosselin et al., 1990) or, perhaps, simultaneously across dense algal layers with steep resource gradients (e.g. Smith et al., 1988; Cota and Home, 1989). Although irradiance and nutrient flux have the same orientation in planktonic and sea ice systems, the relationship between these resources is markedly different in these two systems. In actively mixing waters, phytoplankton experience large vertical excursions in an exponentially decreasing irradiance gradient, whereas ice algae are virtually fixed in the light gradient. Hence, vertical mixing in ice-covered systems may alter the nutrient flux, but not irradiance. Variations in mixing rates and nutrient flux are known to influence ice algal nutrient status and physiological performance in established populations.

Irradiance

Despite its critical importance for biological production at the seasonal sea-ice water interface, irradiance in ice-covered conditions is probably the most poorly measured environmental variable. Problems associated with irradiance measurements will first be examined, before discussing the

264

COTA

significance of temporal and spatial variations in irradiance for the production of ice algae.

,5-,7A~,L,9~3

ET AL

3-4 ~AY,~3

[ SNOWDEPTH ]~-0158

o.~-T-7---- ~

~-0.2,~

0.433 ~

I .........

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I-0"125~' I ~%-~NDE~RA-~II~E[CHLOROPHYLL J0""8 .

Measurements In ice-covered conditions, irradiance is routinely measured under the ice sheet (Eo), at some distance from the hole through which the instrument is lowered. This can be accomplished using divers (e.g. Gosselin et al., 1990), a mechanical arm deployed under the ice (e.g. Smith et al., 1988; Welch and Bergmann, 1989), a moored instrument (Legendre and Gosselin, 1991), or a remotely operated submarine vehicle. Since irradiance is measured beneath the ice sheet, which contains the ice algae that sometimes reach very high concentrations (especially in the bottom few centimeters, e.g. Poulin et al., 1983; Welch and Bergmann, 1989), a large proportion of the photons impinging on the algae may be intercepted by the photosynthetic pigments. The irradiance routinely measured under the ice is thus "contaminated" by the presence of microalgae (Maykut, 1985; Palmisano et al., 1987; Soohoo et al., 1987). In most papers, the problem is simply ignored. However, there have been a few attempts to address this critical problem. Welch and Bergmann (1989) systematically measured irradiance under (E~) and above (Ea) the bottom-ice algal layer (the latter after scraping away the algae). They derived an empirical relationship (Fig. 2a), relating the fraction of irradiLO~,.

0 0.4 ILl ~ll:J0.3

0

/.

b -- 32

a.-,

-p

E

o E --I

•

-F

(J -3 9 4

o

i,

-i

_J

-o ~, --i 0.1

0

40

80

~20

Chl~'(~hyll o (rag m-2)

MARCH

APRIL MAY JUNE

Fig. 2. (a) Percentage of irradiance intercepted by the ice algal layer ( E u / E a ) as a function of in situ biomass (chlorophyll a). (b) Seasonal changes in bottom-ice chlorophyll a (means + 95% C.I.) at various low-snow sites in Barrow Strait, Canadian High Arctic (from Welch and Bergmann, 1989).

~

I~CE THICKNESS] .0.348

I -o.,.7 i'

/'

I ......

I

lICE THICKNESS[/-0.644

Fig. 3. Path diagrams of possible causal relations (arrows) between snow depth, ice thickness, chlorophyll a concentration and underice irradiance, in southeastern Hudson Bay, Canadian Arctic, April-May, 1983. Values of the path coefficients from snow depth and ice thickness to chlorophyll reflect the changing response of ice algae to irradiance as the season progresses (adapted from Gosselin et al., 1986).

ance passing through the ice algal layer (Eu/E,) to in situ biomass (chlorophyll a; Chl):

Eu/E a = 1.102 - 0.196 ln(Chl) This relationship explained 90% of the observed variation over two sampling seasons in Barrow Strait (Canadian High Arctic). Additional measurements should be conducted to establish the universality of the above equation before it is applied to other polar environments. In the mean time, when the concentration of chlorophyll a is known, Welch and Bergmann's (1989) equation could be used (with some caution) to back calculate the irradiance impinging on ice algae (Ea) from measured Eo. An indirect approach to the same problem was used by Gosselin et al. (1986), within the context of explaining the horizontal patchiness of ice algae in southeastern (SE) Hudson Bay (Canadian Subarctic). Using field measurements of snow depth, ice thickness, chlorophyll a and underice irradiance, they computed path coefficients for the causal model shown in Fig. 3. In this model, under-ice irradiance (E u) results from the attenuation by the snow-ice cover and by chlorophyll a. The control exerted by the snow-ice cover (i.e. E a) on the distribution of microalgal biomass corresponds to the paths (arrows) from snow depth and from ice thickness to chlorophyll a. Path analysis is derived from multiple linear regression. Using standard multiple linear regression in conjunction with a simple model of irradiance attenuation by the ice sheet, Smith et al. (1988) were able to explain most of the spatial and temporal variations of under-ice irradiance in Resolute Passage (a tributary channel of Barrow Strait,

ECOLOGY OF BOTTOM ICE ALGAE, I

Canadian High Arctic). Their model includes irradiance (quanta m - 2 s- 1) measured under (Eu) and above ( E ' ) the ice sheet, dimensionless parameters for reflection (a) from bare ice and (c) from snow ( X = 1) versus bare ice ( X = 0), diffuse attenuation coefficients (m - ] ) for ice (ki) and snow (ks), thickness (m) of ice (Zi) and snow (Zs) and the mean specific absorption coefficient (m 2 m g - 1) for chlorophyll a (kch I ) combined with the areal concentration (mg m -2) of chlorophyll a (Chl):

ln( E . / E ' )

= - [ a + ( c X ) + ( k i Z i ) ~t_ (ksZs)

+ ( ch,Cht)] The model explained 93% and 83% of the observed variation, in, 1985 and 1986, respectively and values of the physical parameters (a, c, k i, ks) were fairly similar for the two years. This equation thus provides a means for computing the irradiance impinging on ice algae (Chl = 0), even without knowing their concentration, provided that the various physical parameters have been estimated. As for the equation of Welch and Bergmann (1989) above, similar measurements are required in other sea ice environments in order to estimate the variability of the physical parameters. Another possible way of estimating the attenuation caused by chlorophyll a is to use the spectral distribution of underice irradiance. It is well known that chlorophyll pigments preferentially absorb in the blue and red parts of the visible spectrum, so that there is generally minimum absorption of green light (ca. 520 nm) by microalgae. The ratio of underice irradiance at a wavelength where absorption by algae is maximum to a wavelength corresponding to minimum absorption could thus provide an index of irradiance intercepted by the ice algal layer and, simultaneously, of in situ algal biomass. This idea was tested by Legendre and Gosselin (1991) using under-ice spectroradiometric data of downwelling irradiance (moored 2~r collector) recorded during the spring of, 1986 in southeast Hudson Bay. The ratio of irradiance at 671 to 540 nm was compared to total ice-algal biomass (bottom ice plus icewater interface) measured at a nearby station (Fig. 4). The figure shows that there is a linear relation-

265

0.50 0

a•ix2

= 0,49 - 0.01 x 1

0.45 w 0 Z < m a

•

O.40

o.35

.1 0~" Ill a. ¢n

0.30

; p < 0.05

0.25 CHLOROPHYLL a

(rag m-2 )

Fig. 4. Ratio of underice irradiance at 671 to 540 nm, plotted as a function of algal biomass (chlorophyll a concentration in bottom ice and at the ice-water interface) in southeastern Hudson Bay, Canadian Arctic, April-May 1986 (from Legendre and Gosselin, 1991).

ship between the two sets of measurements, which explains 55% of the observed variation even though the data cover only a short period (23 April-15 May) and were not taken at exactly the same station. A different measurement problem concerns the use of 2~r (flat-circular) versus 4~r (spherical) photon collectors. In the water colunm and in incubation bottles, the photons impinging on algal cells come from all directions, so that a 4~r collector is preferable. However, in environments where algae are concentrated in a thin layer, as is the case for bottom interstitial ice assemblages, it may be argued that a 2 ~r collector is more effective in measuring the irradiance passing through the ice sheet (e.g. Smith et al., 1988; Welch and Bergmann, 1989). This may be especially important since light transmitted through the ice seems to be highly collimated and emerges from the undersurface within 30 ° of the vertical (Buckley and Trodahl, 1987). In areas such as SE Hudson Bay where a significant proportion of the biomass consists of sub-ice algae floating at the ice-water interface, a case could be made for using a 4~r instrument (e.g. Gosselin et al., 1990).

Seasonal variations There are several examples in the literature of parallel increases of under-ice irradiance ( E , ) and ice-algal biomass or production. Since E , is negatively affected by the photosynthetic biomass in

266

COTA

In Barrow Strait, Welch and Bergmann (1989) observed an exponential increase of chlorophyll a in bottom ice at most of their low-snow sites (Fig. 2b). Combining all their sampling sites, the irradiance at the surface of the ice (cumulated since the return of light in February) combined with snow depth explained 60-80% of the variance in the bottom-ice chlorophyll a. In the same area, Smith et al. (1988) stabilized the snow cover with a snow fence (which anchored the snow drift and prevented drift migration). This resulted in a stable drift with a central apex at 30 cm height sloping down over 5 - 7 m to a height of 2 - 4 cm; in addition, a cleared patch of ice was kept relatively free of snow with a snow blower (see Cota, 1985). Observed seasonal increases in bottom-ice microalgal chlorophyll, under four different depths of snow cover (Fig. 6a), corresponded well to the maximum biomass computed using the parameters of their irradiance attenuation model (above) together with measured photosynthetic parameters and solar irradiance. This confirms the role of irradiance in controlling ice-microalgal biomass, even if somewhat lower values than predicted were observed under the thin snow cover (discussed below). Concerning rnicroalgal production in southeastern Hudson Bay, Gosselin et al. (1990) observed light-limited carbon uptake during the first part of the growth season, followed by silicon limitation. This led to a seasonal increase of both under-ice

• ,oo i

-

o~ - - ~ ~o'

e6o

' aod

4oo

e6o

oo

4oo

coo

coo

Wavelength (nrn) Fig. 5. Percentage of surface irradiance [E'(X); spectral distribution] transmitted through first-year ice as a function of ice thickness, for (a) blue ice covered by melt pond, (b) white ice and (c) blue ice overlain by a 25 cm layer of melting snow (after Maykut and Grenfell, 1975).

bottom ice a n d / o r at the ice-water interface, any positive correlation with microalgal variables is indicative of a strong biological response to irradiance. Concerning seasonal variations in the spectral distribution of under-ice irradiance (~: wavelength), Maykut and Grenfell (1975) calculated that the percentage of E ' ( X ) transmitted through first-year ice as a function of ice thickness for (a) ice covered by melt pond and for blue ice (ice saturated with water at the local water table), (b) white ice (melting ice, above the local water table and continuously drained) and (c) for blue ice overlain by a 25 cm layer of melting snow. Their results (Fig. 5) indicate that all cases exhibit strong attenuation in the red and that maximum transmission through first-year ice is in the 450-550 nm region (blue-green, regardless of surface conditions or ice thickness).

--

°-

tJ 2

o

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~ ="

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,

,

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Dates

°°

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.•

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ET AL.

, MAY

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u.,, APRIL

,

, MAY

• APRIL

MAY

Dates

Fig. 6. Seasonal changes in biomass indices under four different show depths (0, 2-4, 8-12 and 18-22 cm). (a) Bottom-ice chlorophyll a; solid lines are computed maximum biomass (b) Particulate organic carbon; the solid lines are cumulative POC computed from net photosynthetic carbon. Points (dots) are observed values in Barrow Strait, Canadian High Arctic, April-June, 1985 (after Smith et al., 1988).

ECOLOGY OF BOTTOM ICE ALGAE, I

267

~o, so

~ 4o d

2O 0

' E 1.6 ~o. Q.

5

15 25 APRIL

5 MAY

15

Dotes

Fig. 7. Seasonal variations in underice irradiance (E u) in situ primary production and particulate organic carbon (POC) at the ice-water interface,in southeastern Hudson Bay, Canadian Subarctic (after Gosselin et al., 1990a). irradiance and in situ carbon uptake by the ice algae, but no strict parallelism (Fig. 7). Particulate organic carbon (POC) also increased seasonally, but when the availability of silicon became limiting, the algae used the higher irradiance more for storage of photosynthates than for growth (Gosselin et al., 1990). Smith et al. (1988) compared observed POC in Resolute Passage to cumulative POC calculated from net photosynthetic carbon production rate (Fig. 6b). The values, somewhat lower than predicted observed under thin snow cover for both POC and chlorophyll a (Fig. 6a), were explained by increased losses from the clear ice populations, perhaps through excessive energy absorption and consequent deterioration of the ice. This means that production under the thinnest snow cover was poised between limitation by irradiance and irradiance excess. The same phenomenon may be instrumental in ending the ice algal bloom (Horner, 1985a). Horizontal variations

As mentioned above for Barrow Strait, Welch and Bergmann (1989) were able to explain 60-80%

of the variance in the spatio-temporal distribution of the b o t t o m - i c e algal biomass by the irradiance impinging on ice microalgae (i.e., cumulative surface irradiance after the return of light combined with snow depth). This is an indication that irradiance may be the major environmental factor controlling the spatial distribution of ice algae. A more experimental approach was used in the same area, where snow cover was stabilized with a snow fence (see above). Figure 8 shows the importance of snow depth on irradiance transmitted through the snow-ice sheet (ice thickness varied little during the study). Using these data, together with measured photosynthetic parameters and solar irradiance, Smith et al. (1988) computed the maximum biomass for each snow depth, which ranged from 75-80 mg Chl a m 2 (for 0 and 2 - 4 cm snow) to 55-60 (8-12 cm) and to 30-35 (18-22 cm). Corresponding annual ice algal production rates, for the same four snow depths, were 5.8, 6.1, 3.3 and 1.2 g C m -E, respectively (50-d growth season). Somewhat similar conclusions were reached by Gosselin et al. (1986), who sampled ice cores every 5 m along 500 m transects (perpendicular to snow drifts) in SE Hudson Bay, together with environmental variables. Snow played a more important role in April (average 15 cm) than in May (3 cm). The signs of the relationships between the thickness of the snow-ice cover and chlorophyll a concentration (Fig. 3) changed from negative (April) to positive (May); this was explained by a seasonal change in the photosynthetic characteristics

~-

5

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10-22 cm 6-12 cm~ 20

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60

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Fig. 8. Underice transmittance versus areal chlorophyll a concentration, under 4 different snow depths (0, 2-4, 8-12 and 18-22 cm), observed in Barrow Strait, Canadian High Arctic, April-June, 1985; the solid lines correspond to the fitted irradiance attenuation model (from Smith et al., 1988; Fig. 2).

268

of ice algae, which were light limited in April (growth limited by low irradiance under thicker snow-ice cover) and susceptible to photoinhibition in May (thicker snow-ice cover then providing shelter from inhibiting irradiance). Harmonic analyses indicated that the horizontal structures of ice microalgae were of the order of 20-30 m, as were those of snow depth and ice thickness. Nutrients

Because most polar waters are relatively nutrient rich, it was usually assumed that supplies were not limiting for ice algae. However, nutrient availability apparently limits ice algal biomass accumulation and alters physiological performance or biochemical composition of microalgae in fairly predictable ways. Numerous recent studies have concluded that the availability of inorganic nutrients may limit ice algal production, particularly when biomass levels are elevated during the latter stages of blooms. Nutrient limitation in ice algal populations has been inferred from nutrient distributions and ratios (Meguro et al., 1967; Grainger, 1977; Cota et al., 1987, 1990), final yields of biomass in differential enrichment bioassays (Maestrini et al., 1986; Gosselin et al., unpubl.), budgets of requirements and supplies (Cota et al., 1987; Cota and Horne, 1989; Demers et al., 1989; Cota and Sullivan, 1990), photosynthetic performance (Gosselin et al., 1985; Smith et al., 1987; Cota and Horne, 1989; Cota and Sullivan, 1990), patterns of photosynthate allocation (McConville, 1985; Palmisano and Sullivan, 1985; Smith et al., 1987) and biochemical composition (McConville, 1985; Demers et al., 1989; Smith et al., 1989b; Gosselin et al., 1990). In SE Hudson Bay the limiting nutrient apparently changes along a salinity gradient due to an alteration in the balance between horizontal advection and vertical mixing: at very low salinities (ca. 5 g/kg) phosphorus is limiting, while at intermediate (17-27) and high salinity ( > 25) the limiting nutrient changes from nitrogen to silicon (Gosselin et al., unpubl.). The potential for silicon limitation in sea ice systems in fully marine waters has been emphasized in high latitude studies (Cota et al., 1987, 1990; Cota and Sullivan, 1990).

COTA ET AL.

Measurements

Nutrient measurements are difficult to obtain in sea ice systems and most observations are relatively crude, pertaining only to bulk concentrations in ice or seawater. At present, we can not easily segregate nutrients from melted ice cores into those derived from ice, brine and organisms. Nor can we describe nutrient distributions and dynamics over appropriately small scales characteristic of the ice algae's microenvironment(s). Again, difficulties associated with measurements are dealt with before discussing the variability of nutrient supply. Because sea ice columns usually experience a temperature gradient (ca. linear from air to water) and they are two-phase systems composed of ice and interstitial brines in pockets, tubes and channels, ideal measurements would determine microscale nutrient concentrations in each of these distinct regions. The presence of algal contaminants further complicates the picture because they may act as a strong nutrient sink (Cota and Home, 1989) and often have substantial intracellular pools of soluble nutrients (Cota et al., 1990; Gosselin et al., unpubl.; Smith et al., 1990). " N e w " nutrients potentially available to ice algae are found both in seawater and in ice, so concurrent measurements should be made on both. However, most observations have been made on melted core segments a few to many centimeters long or seawater samples collected with 2-5 L bottles (ca. 20-70 cm long). To improve our understanding of the ice algae's microenvironment(s) we need new technical approaches to measure concentrations, gradients and fluxes over the appropriate scales in ice and water with minimal perturbation of the environment. An indirect method to achieve some of these aims is described by Legendre et al., 1991. Nutrients may be supplied to ice algae by three principal mechanisms: desalination (brine rejection and drainage), regeneration or vertical diffusion from the water column (Meguro et al., 1967; Cota et al., 1987). Each mechanism is dealt with in turn. Sea-ice structure is complex and has a specialized terminology; the reader should consult Weeks and Ackley (1982) and Maykut (1985) for more comprehensive discussions of sea ice. Several important structural features and processes of the

ECOLOGY OF BOTTOM ICE ALGAE, 1

NITRATE (mmol m" 3) 5 i I i

0

02

L ~,~ %%

E

o

10 I

I~

I

/"x SURFACE

\'

,M2x~ LAYER II

I I

'

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269

|~, U

MIXED LAYER

-',

- - ~ BRINE CHANNEL ,,Y " SYS'rEM~ . ~ / / ',

-"

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which relates nutrient demand D, (mmol m -2 d - 1) to the observed rate of biomass accumulation as the product of growth rate # (d-1) and algal biomass B, in terms of a nutrient element (e.g. nitrogen or silicon in mmol m 2) (Cota and Horne, 1989). Such estimates of demand are conservative because loss terms are not considered but allow us to place an approximate lower bound on the supply of " n e w " nutrient required to sustain a bloom's continued growth.

Desalination nutrient supply

100

~kJ//

t 0

I 10

I

vISCOUS SUBLAYER ~ 0.Ecm

I 20

I

I 30

1%

SILICIC ACID (mmol m- 3) Fig. 9. S c h e m a t i c of s t r u c t u r a l f e a t u r e s a n d p r o c e s s e s in sea ice

and water column (drawing adapted from Harrison and Cota, 1990; not to scale). Heavy solid line on left shows nutrient distributions in ice and water columns for Barrow Strait, Canadian Arctic; density shows the same pattern in the water column. Heavydiagonal (dashed) line illustrates nutrient gradient that is frequently observed in surface mixed layer (after Cota and Home, 1989). Open elipsoids with arrows represent relative scales for vertical mixing in each layer. Square inset shows interior brine channels and brine tubes in skeletal layer. Circular inset illustrates the flows patterns for skeletal layer convection (arrows on left side), brine drainage plume from a brine channel (center) and velocity profile (right side below interface; dots represent location of horizonital velocity U measurements and line shows linear portion near boundary) across viscous sublayer. ice or water columns are shown schematically in Fig. 9 (drawing not to scale). Spatial and temporal considerations are stressed to illustrate where, when and how much nutrient is made available by these processes. To ascertain the adequacy of a particular source of nutrients, we need knowledge of relative fluxes of sources and sinks. Minimal nutrient fluxes necessary to support ice algal blooms can be estimated from: D, =/LB,

Desalination processes include brine exclusion or rejection during the formation of ice and subsequent brine drainage. Most of the salt (ca. 70%) is rejected from the interfacial skeletal layer during ice formation or shortly thereafter, but brine drainage from the interior of the ice column continues throughout the life of the ice sheet through networks of brine channels (Lake and Lewis, 1970; Weeks and Ackley, 1982) (Fig. 9). Nutrient salts in annual or first-year sea ice are largely conservative with respect to salinity except in the bottom few em of ice where concentrations of nitrogen and phosphorus, but usually not silicon, may be greatly elevated; the degree of enrichment is directly proportional to algal biomass and appears to reflect stored intracellular pools (Cota et al., 1990; Smith et al., 1990). Ice structure and the distribution of algae have important implications for nutrient availability. It has often been stated erroneously that bottom interstitial algae live primarily in brine pockets and channels and that brines in or draining from the ice sheet are likely an important source of nutrients (e.g. Palmisano and Sullivan, 1983; Grossi et al., 1984). Although brine pockets are widely distributed in sea ice, brine channels are discreet features and comprise a very small portion of the surface area of bottom ice (see below). Only a very small percentage of cells in bottom interstitial assemblages actually occur in brine pockets and brine channels per se; most cells are dispersed over the entire bottom surface in small brine tubes and less regular features in the skeletal layer. Therefore, most cells are in contact with surface seawater. Compared with rubbings of the bottom of uncolonized sea ice (cf. Weeks and

270

Ackley, 1982), heavily colonized annual ice in the high Arctic is much more irregular with small "craters" and visible clumps of algae are scattered over these depressions which the algae presumably create themselves (Cota, unpubl.). The structural characteristics of sea ice provide a good basis for understanding the potential importance of desalination processes in promoting nutrient fluxes on scales most applicable to ice algal populations. Two processes, skeletal layer convection and brine channel convection, are of particular interest because they promote fluxes, in excess of molecular diffusion, across the viscous sublayer. However, these two processes occur over different time and space scales. The bottom skeletal layer of congelation ice has thousands of small brine tubes m -2 (42 cm -2 in 1.6 m thick ice); they have average diameters of 0.1-0.4 mm and extend 0.4-3 cm into the ice with laboratory values representing the lower end of the range (Lake and Lewis, 1970; Niedrauer and Martin, 1979). Brines flowing out of the skeletal layer of growing sea ice create small cyclic convective events with diffuse inflows of seawater and intense downward plumes of brines at cusps spaced about 1 cm apart (Fig. 9) (Lake and Lewis, 1970; Niedrauer and Martin, 1979). Skeletal convection should enhance nutrient fluxes from the water column over most of the lower margin, but the brine plumes, which are nutrient-rich, appear to maintain their integrity as they leave the ice. Brines would have to be remixed with seawater and transported vertically to become available to bottom ice algae. Convection in the skeletal layer is operative only while salts are being excluded when the ice sheet is growing (Reeburgh, 1984) and corresponds to about the first half of algal blooms. By contrast, brine channels are three dimensional branching tributary systems which penetrate the interior of the ice sheet; the central vertical channels are usually 0.5-1.0 cm in diameter, but they are discrete features with only about 50-200 m -2 (Lake and Lewis, 1970; Wakatuschi and Ono, 1983). Cold brines draining from rapidly growing (1.5-12.2 cm d -1) new ice have salinities of about 42-93 and the brine flows out of the ice at a few specific sites in long vertical filaments or streamers which fall into the underlying water without ap-

COTA ET AL.

preciable diffusion in at least the upper 10-20 cm (Wakatsuchi and Ono, 1983). Therefore, convective fluxes associated with brine channels, whether oscillatory (intermittent) or continuously bi-directional (Niedrauer and Martin, 1979), are largely point sources at the mouths of brine channels. Brine streamers exciting the ice from channels would have to be mixed laterally and vertically to be of much value to most bottom interstitial ice algae and seawater flowing into brine channels to maintain continuity has much lower nutrient concentrations than brines. On the other hand, the diffuse inflows of seawater associated with skeletal convection appear to be of the proper spatial scale. Volume fluxes of brines from exclusion and early drainage appears to be proportional to the rate of accretion in new ice (Wakatsuchi and Ono, 1983). We are unaware of spring field studies quantifying convective fluxes resulting from brine expulsion and drainage, so the magnitude and seasonal dynamics of these processes can only be estimated. Observed volume fluxes from thin ( < 15 cm) ice growing at 1.5 cm d-~ in the laboratory are only 6.3- 10 -6 ml cm -2 s -~ (Wakatuschi and Ono, 1983), whereas Reeburgh (1984) estimated that fluxes of 2 0 - 7 0 0 . 1 0 - 6 ml cm -2 s -1 were necessary to meet observed nitrogen uptake rates (i.e. 0.13-0.60 mmol m -2 d -1) for low to moderate levels of algal biomass (2.5-23 mg Chl m -2) on ice about 1.6 m thick (Alexander et al., 1974). At other high latitude sites, with relatively high biomass ( > 50 mg Chl m-2), values for observed or predicted nutrient uptake rates for ice algae often range up to an order of magnitude or more higher (i.e. 3-21 mmol m -2 d -~) (Cota et al., 1987; Cota and Home, 1989; Cota and Sullivan, 1990; Harrison et al., 1990). Based on several studies in SE Hudson Bay (Gosselin et al., 1985; Barlow et al., 1988; Michel et al., 1988), maximum estimates of nutrient demand for nitrogen or silicon are < 2 mmol m - 2 d-1 (Cota, unpubl.). Reeburgh (1984) suggested that volume fluxes of brines from skeletal layers were between 10-4 and 10 -8 ml cm -2 s -1, but the only empirical data available was obtained from rapidly growing, thin new ice in laboratory studies and values ranged up to 3.4.10 -5 ml cm -2 s -1 for ice 5-8 cm thick

ECOLOGY OF BOTTOM ICE ALGAE, I

growing at a rate of about 12 cm d -x. During vernal ice blooms, ice sheets are usually 1-2 m thick and grow at mean rates < 1.0 cm d-a during the early stages of blooms (e.g. Gosselin et al., 1985; Cota et al., 1987; Welch and Bergmann, 1989; Cota and Sullivan, 1990). Given that convective fluxes in nature are probably even lower than the minimum laboratory observations cited above and occur only during the exponential growth phase, it appears that volume (and nutrient) fluxes driven by convection below growing sea ice are often 2-3 orders of magnitude lower than nutrient demand. Utilizing a dimensional analysis consistent with McPhee and Smith's (1976) for the influence of convection under arctic pack ice, Cota et al. (1987) suggested that convective mixing under landfast ice in Barrow Strait might be significant during the early phases of the algal bloom when the ice sheet is still accreting. However, since the mean growth rates of the ice were low in early spring and fell to zero around mid-bloom, they concluded that convective mixing was probably of secondary importance to turbulent mixing driven by the flows under the ice (see below). The potential nutrient supply derived solely from salts trapped in the ice during the spring bloom can be estimated by integrating nutrient profiles of ice near the end of the ice growth season (Cota et al., 1987, 1990; Cota and Sullivan, 1990). The amount of silicic acid or nitrate in the entire ice sheet is roughly equivalent to that in the top 0.3-0.5 m of the water column. If all nutrients in the ice were available to the bottom ice cells during the bloom (an unreasonable assumption, because they are "locked" in the ice sheet until the melt), moderate levels of algae would deplete this supply in a week or two of rapid growth. The largest pulse of nutrients from ice occurs when the ice starts to melt in late spring and is more or less coincident with the demise of the bloom. Nutrients from the ice sheet represent only a small portion of the bloom's minimum demand for nitrogen and silicon over the 45-90 day spring bloom (Cota et al., 1987; Cota and Sullivan, 1990).

Regenerative nutrient supply Regenerative nutrient fluxes within sea ice sys-

271

tems are virtually unknown. Regeneration of nitrogen and phosphorous presumably contributes substantially to the required supply, but silicic acid is normally "regenerated" much more slowly by dissolution and may be exported as particulate biogenic silica (Nelson and Gordon, 1982; Cota and Sullivan, 1990). Uptake and regeneration rates 15 of N-ammonium were about equal in bottom interstitial assemblages of McMurdo Sound, Antarctica (J.C. Priscu, pers. commun.), but average f-ratios ( f = pNO3/(pNO 3 + pNH4) were around 0.5, suggesting that half of the nitrogen utilized was nitrate (Cota et al., unpubl.). Similar patterns of nitrogen utilization also have been reported for ice algal communities in Hudson Bay (Gosselin et al., unpubl.) and in the high Arctic, where nitrate reductase activity was not suppressed even at very high ammonium concentrations (Harrison et al., 1990). Employing relationships for weight-specific rates of nitrogen (ammonia) excretion, Cota et al. (1987) estimated that regenerated nitrogen satisfied only a small portion of the N required for the algal bloom. Much needs to be done to quantify the relative importance of regenerative fluxes for all of the major nutrients (i.e. N, P and Si). The structure and organization of sea ice systems presents special challenges, because much of the biomass is on or under the ice which is difficult to study intact in situ and part is exported to motile grazers or the water column and benthos. Therefore, some recycling occurs within ice algal layers and in the water column or benthos. Within bottom interstitial layers, the availability of regenerated N and P will presumably be largely a function the abundance, size distribution and type of heterotrophs. The two basic types include small "infauna" living in the ice (e.g. bacteria, nematodes) and larger "epifaunal" organisms moving over the surface (e.g. amphipods, copepods). Although pre-existing populations of epifauna may colonize the ice at the onset of a bloom, most heterotrophs increase seasonally in parallel with autotrophs. Bacteria and other infauna usually comprise only a small percentage of ice algal biomass (Cota et al., 1987; Kottmeier et al., 1987; Smith et al, 1989a). With relatively high weight-specific excretion rates and abundance, small infauna are likely to be the most

272

important source of regenerated nutrients. In contrast, if epifauna excrete into seawater, their excretion products will be less available to interstitial algae due to rapid dissipation and their weightspecific rates of excretion and abundance are much lower (Cota et al., 1987).

Water column nutrient supply Comparisons of total nutrient requirements to satisfy ice algal blooms and concentrations of inorganic nutrients in the water underlying the ice typically indicate that more than ample quantities of nutrients [nitrogen, phosphorus and silicon in the form of NO3, PO 4 and Si(OH)4 , respectively) exist in the water column (Cota et al., 1987; Cota and Horne, 1989; Cota and Sullivan, 1990; Table 1). For example, the total silicon required for ice algal blooms can usually be supplied by the Si(OH)4 in the upper few meters of the water column. Nutrient concentrations in McMurdo Sound are relatively high, but density stratification is normally very weak (Table 1). If it exists, the surface mixed layer is usually much deeper (i.e. > 50-100 m) (Littlepage, 1965, Lewis and Perkins, 1985), so nutrient depletion is less likely to be detectable (Cota and Sullivan, 1990). In the high Canadian Arctic concurrent observations of density and nutrients show steep and persistent gradients for both nitrate (NO3) and silicic acid [Si(OH)4 ] across the otherwise "well-mixed" surface layer; a strong source-sink relationship for nutrients is implied by the steep gradients across the "mixed" upper layer (Cota and Home, 1989). In SE Hudson Bay concentrations of N O 3 and Si(OH)4 are several times lower (Gosselin et al., 1985, 1990) than in Barrow Strait (Cota et al., 1990). Data in Table 1 illustrate how increased stratification in the low energy regime of SE Hudson Bay can reduce upward nutrient flux in contrast to Barrow Strait and McMurdo Sound. The stratified waters found in southern Beaufort Sea are expected to moderate nutrient fluxes in a similar fashion as that occurring in SE Hudson Bay (Aagaard and Carmack, 1989). In ice-covered systems, scalar properties such as inorganic nutrients may be mixed vertically by convection arising from brine rejection a n d / o r

COTA ET AL.

drainage from the ice sheet (Lake and Lewis, 1970; Niedrauer and Martin, 1979; Reeburgh, 1984), by turbulence resulting from shear instabilities in and from, drag on the tidal and other flows under the ice (Gosselin et al., 1985; Cota et al., 1987; Carmack, 1986) or by entrainment and mixing due to internal waves or topographical features (Ingram et al., 1989). The importance of tidally induced vertical mixing in the supplying nutrients to the ice algae in the Subarctic (Gosselin et al., 1985) and in the Arctic (Cota et al., 1987) has been considered previously and can be illustrated with simple biological and physical models. Biological demand for nutrient(s) must be less than or equal to physical supply when production is based on nitrate or silicic acid (Cota and Horne, 1989; Cota and Sullivan, 1990). Vertical nutrient fluxes can be estimated with the gradient transport hypothesis and the flux F n can be obtained from F n = Kz(An/Az

)

where K Z is the vertical eddy diffusivity (m -2 d -1) and An is the difference in nutrient concentration over the vertical interval Az of interest (mmol m -4) (Cota et al., 1987). In Barrow Strait, variations in maximum current speeds are largely dependent upon tidal forcing with the fortnightly cycle evident in the current regime and in calculated eddy diffusivities (Fig. 10; Cota et al., 1987). Hence, all observations were related to the tidal height data which are generally available and reliable for many regions. Becasue consumption of the magnitude estimated would noticeably deplete a shallow surface mixed layer (of order 10 m and 2 m thick for Barrow Strait and SE Hudson Bay, respectively), the replenishment of Si(OH)4 from the pycnocline, as well as the mixing rates across it, were also considered; nutrient fluxes across density gradients are much lower even if the nutrient gradients are comparable (Cota et al., 1987). Although the relationships did not hold for surface mixed layers, gradients of nitrate and silicic acid in the pycnocline were related to tidal range as a function of time, R(t), with time lags. These gradients sharpen as the thickness of the pycnocline decreases with the increased shear found during the stronger

ECOLOGY

273

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spring tidal currents (Cota et al., 1987; Cota and Horne 1989). Because nutrient fluxes are subject to physical and biological variability, nutrient limitation is not easily proven in nature. Nutrient concentrations are usually measured over much larger scales than the ice algae's microenvironment and can be misleading. If demand is comparable to supply, then fluxes may be high even when concentrations are relatively low and vice versa. Nutrient concentrations in surface water and skeletal ice are rarely low enough to be considered limiting (Cota et al., 1990), but the fluxes in the upper water column may vary by an order of magnitude or more, as can demand (Cota and Horne, 1989; Cota and Sullivan, 1990). The ice sheet is not growing during the latter part of the algal bloom and convective flushing of the skeletal layer, which results from brine rejection at an accreting interface, should be absent or greatly diminished (Reeburgh, 1984). Furthermore, the nutrient uptake characteristics of these ice algae are not well known; they may have low affinities (i.e. relatively large half-saturation constants) for nutrient up-

take (Jacques, 1983; Maestrini et al., 1986; Sommer, 1986). The actual nutrient concentrations and fluxes in the algae's microenvironment(s) have yet to be determined. Suitable new technologies must be employed to examine fluxes on scales of m to mm to resolve this question. Bottom ice algae colonize the interstices of the skeletal layer (scales of < 1 mm to 3 cm) of the ice sheet and their nutrient supply is ultimately limited by molecular diffusion across the viscous sublayer, the linear region of the velocity profile near the boundary. Recent measurements in the Arctic reveal that the non-dimensional thickness of the sublayer is thicker than expected, in the range of 3-6 mm (Conover et al., 1990; E.P.W. Horne, pers. commun.). Rates of nutrient supply directly to the algae will be largely a function of the diffusion gradient across the sublayer, the velocity near the boundary (Fig. 9) and the thickness of the sublayer. Algal consumption will steepen the gradient and regeneration in the bottom ice will tend to weaken it. Vertical mixing in the surface mixed layer will also steepen the gradient by maintaining higher concentrations below the sublayer. Hence, if demand equals supply, then the gradient across the viscous sublayer will remain steep.

Concluding remarks Environmental conditions and their varabilility play important roles in the ecology of ice algae. There are marked regional differences in environmental conditions at the four sites considered above (Table 1), which contribute to differences in the types of ice algal assemblages at each location and their maximum biomass. Bottom interstitial assemblages were common to all of the sites, but sub-ice assemblages were not. For example, in SE McMurdo Sound supercooling creates the frazil ice layer which is absent at most other locations. Climatic differences between subpolar and polar sites can be pronounced. Bloom periods tend to be longer above polar circles because photoperiods are longer, air temperatures remain lower longer and ice abaltion is later. Hence, biomass has longer to accumulate. The lowest maximum biomass was observed in SE Hudson Bay, the area which had

274

the shortest b l o o m p e r i o d , the least saline waters and generally lower nutrient concentrations. R a p i d l y rising air t e m p e r a t u r e s in m i d - M a y at this low l a t i t u d e l e a d to an earlier s p r i n g melt. I n spite of these differences, SE H u d s o n B a y a n d the s o u t h e r n Beaufort Sea are generally q u i t e similar. Both are low energy e n v i r o n m e n t s ( c h a r a c t e r i z e d b y velocity) with significant vertical stratification. M a x i m u m b i o m a s s e s were lower at these locations. In a similar fashion, c o n d i t i o n s in B a r r o w Strait a n d M c M u r d o S o u n d were c o m p a r a b l e . W e a k stratification a n d / o r a higher energy env i r o n m e n t lead to higher b i o m a s s e s t h a n at the o t h e r two locations. W i t h salinity a n d t e m p e r a t u r e effectively cons t a n t over m o s t of the b l o o m period, b o t t o m a n d sub-ice ice algae m u s t o p t i m i z e their use of available i r r a d i a n c e a n d nutrients. E x c e p t i n g v a r i a t i o n s in snow cover (deposition, e r o s i o n o r melt), the light e n v i r o n m e n t is relatively c o n s t a n t , in contrast to p l a n k t o n i c p o p u l a t i o n s where vertical m o tion in the w a t e r c o l u m n results in large fluctuations in light over p e r i o d s f r o m seconds to hours. V a r i a b i l i t y in solar r a d i a t i o n in sea ice systems is m o s t p r o n o u n c e d at diel a n d seasonal scales. I r r a d i a n c e is the m o s t i m p o r t a n t e n v i r o n m e n t a l factor c o n t r o l l i n g the the e x p o n e n t i a l p h a s e of b l o o m d e v e l o p m e n t . W h e n b i o m a s s is high selfs h a d i n g a n d n u t r i e n t a v a i l a b i l i t y m a y limit ice algal growth. N e w n u t r i e n t s are s u p p l i e d p r i m a r i l y f r o m the w a t e r column. N u t r i e n t a v a i l a b i l i t y varies seasonally with ice g r o w t h a n d over s h o r t e r time scales with h y d r o d y n a m i c forcing.

Acknowledgements S u p p o r t from the Office of N a v a l R e s e a r c h (U.S.), N a t i o n a l Science F o u n d a t i o n (U.S.) a n d N a t u r a l Sciences a n d E n g i n e e r i n g C o u n c i l of C a n a d a were i n s t r u m e n t a l in the c o m p l e t i o n of this work. C o n t r i b u t i o n ( M G , R G I , LL) to the p r o g r a m of G I R O Q ( G r o u p e i n t e r u n i v e r s i t a i r e de recherches o c r a n o g r a p h i q u e s d u Q u r b e c ) .

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