Bulletin of Glaciological Research ,1 (,**3) ,/ῌ-/ῌJapanese Society of Snow and Ice

25

ArticleA snow algal community on the surface and in an ice core of Rikha-Samba Glacier inWestern Nepali Himalayas
Nozomu TAKEUCHI+, Koji FUJITA,, Fumio NAKAZAWA-, Sumito MATOBA.,
Masayoshi NAKAWO/ and Birbal RANA0+ Department of Earth Sciences, Graduate School of Science, Chiba University, Japan, Graduate School of Environmental Studies, Nagoya University, Japan- National Institute for Polar Research, Tokyo, Japan. Institute of Low Temperature Science, Hokkaido University, Japan/ National Institutes for the Humanities, Tokyo, Japan0 Department of Hydrology and Meteorology, Government of Nepal(Received July +/, ,**3; Revised manuscript accepted December +., ,**3)

Abstract
A snow algal community on Rikha-Samba Glacier in the western Nepali Himalayas was investigated in October, +332. Examination of surface snow and ice on the glacier revealed that thiscommunity consisted of mainly seven taxa including green algae and cyanobacteria. The algal
community showed an altitudinal distribution on the glacier: its biomass decreased with increasing
altitude and community structure changed with altitude. Snow algae were also found in an ice coredrilled at the top of the glacier. The ice core was +/ m deep and spanned -1 years (+30,ῌ32) based on
the analyses of tritium, dust, and stratigraphy. Snow algae in the ice core included four taxa of snow
algae, which were likely the same taxa observed on the glacial surface. The record showed that thebiomass and species composition of the snow algae varied among layers in the ice core. Some layers
contained algae that were observed only at a lower altitude of the glacier in the studied year. Thisimplies that altitudinal distribution of a snow algal community could shift up or down on the glacialsurface from year to year. Although the variation in this algal community in the ice core might bea#ected by spatial variation and diagenesis of algal cells in the glacial ice, the biomass increase in the+33*s and the variation in species composition are likely to reﬂect an algal community appearing on
the glacial surface.

+.

Introduction

Glaciers are inhabited by specialized organismsthat have adapted to extremely cold environments,
e.g., snow algae, insects, ice worms, copepods, rotifers,
tardigrada, and bacteria. These organisms spend
their whole lives on snow and ice, and they are forming glacial ecosystems, which are simple in terms of
their species diversity and sources of energy and nutrients (e.g., Kohshima, +321; Hoham and Duval, ,**+).
Recently, glacial changes, such as alterations in massbalance, snow chemistry, and/or dust concentration
have been reported in many regions of the world (e.g.,Thompson et al., +33-, ,***), which may a#ect a biological community on the glacial surface. However,
little attention has been given to the total impact on
glacier ecosystems. Also, the biological communities
have a geophysically important e#ect: blooms of the
microbes in snow and ice can reduce the surface al-

bedo and then accelerate the melting of snow and ice(e.g., Takeuchi et al., ,**+; Kohshima et al., +33-). Although the degree of glacial shrinkage is now a matter of concern in response to recent climate change,such shrinkage also may possibly be accelerated froman increase in biological productivity. Thus, the temporal variations in that activity on glaciers are ofgreat interest to the study not only of glacial biology
but also of glacial ﬂuctuations.
Ice core studies could provide a means to reconstruct the temporal variations in biological activity on
the glacial surface. Spores of microbes are usuallydeposited on the glacial surface along with windblown dust in the dry winter season. The microbes
photosynthetically grow later on the wet glacial surface during the summer thawing season, and thenthey are ﬁnally frozen and buried in new snow in thelate summer. They can be preserved every year in
the glacial ice as long as the surface is located in an
accumulation area. Thus, an ice core should provideBulletin of Glaciological Research26

a continuous record of microbes deposited and grownon the glacial surface (e.g., Xiang et al., ,**/; Yoshimura
et al., ,***, ,**0; Willerslev et al., +333). Furthermore,since growth of the organisms depends on physical orchemical conditions on the glacial surface, the biogenic material in ice cores can be expected to constitute a new indicator for interpreting past environments. Biological analysis of ice cores from areas ofheavy melt could be particularly useful since biogenic
materials appear to be less a#ected by meltwaterpercolation due to their larger size, even when stable
isotopes or chemical signals are reduced or eliminated(Yoshimura et al., ,***).
In this paper, we aim to describe the spatial andtemporal variations in the snow algal community
on the Rikha-Samba Glacier in the western Nepali
Himalayas and to demonstrate possible factors a#ecting algal biomass and community structure on theglacier. The altitudinal distribution of a snow algal
community was analyzed qualitatively. The temporal variation in snow algal community for the last
several decades was reconstructed from a shallow ice
core drilled at the top of the glacier. These variations
were discussed with physical and chemical conditions
on the glacier.

,.

Study site and methods,.+

Rikha-Samba Glacier
The research was carried out in October +332 on
the Rikha-Samba Glacier in the Himalayas. The glacier is located near Mt. Dhaulagiri (2+01 m a.s.l.), which
is a summit renowned for mountaineering in western
Nepal (Fig. +). The glacier ﬂows southward from asnowy pass (/3** m a.s.l.) down to the terminus (/-** ma.s.l.). The equilibrium line was located at /2** m a.s.
l., which is based on the mass balance surveys conducted in +332 and +333 (Fujita et al., ,**+a). The
length and area of the glacier are approximately 0.*
km and ..2 km,, respectively. The recent glaciological studies on this glacier have shown a signiﬁcantretreat over the last .* years (e.g., Fujita et al., ,**+a).

,.,Examination of the snow algal community on theglacier
To describe a snow algal community on this glacier, surface snow and ice were examined in accordancewith previous studies on glaciers (e.g., Yoshimura
et al., +331). Collection of surface snow/ice including
snow algae was carried out at the seven sites in thearea between /-/* and /22* m a.s.l. (S+-S1, Fig. +). In
the study period, the entire glacial surfaces were covered with new snow, which likely fell in the monthprior to this study. The depth of new snow increased
with elevation; it was + cm at site S+ and /* cm at site
S1. The sampling was done on the summer glacialsurface below the new snow, on which snow algae

usually grow. The condition of the summer surface
was ice at sites S+-S/ and snow at sites S/-S1. Four
samples were collected from randomly selected surface at each study site with a stainless-steel scoop(cylindrical shape, 00 mm in diameter῍,+/ mm length).
The collected surface ice/snow was approximately /῍/ cm in area and +ῌ, cm in depth. After the collection, the exact area was measured with a ruler tocalculate the amount of the algal volume biomass perunit area. The samples were melted and preserved asa -ῌ formalin solution in clean -*mL polyethylene
bottles within - hours at the base camp (located at thefront of the glacial terminus). These samples wereused for cell counting. Although the ﬁne structure of
the algae in the samples might be lost by formalin, thealgae could still be counted with a microscope. For
identiﬁcation of algal taxa, other samples were collected at each study site and preserved with /ῌ glutaraldehyde solution. The identiﬁcation of the taxa
was done based on mainly Yoshimura et al. (+331),
which is a report on snow algae on a Himalayan
glacier. All samples were transported to the biological laboratory of Tokyo Institute of Technology inJapan for analysis. The algal biomass of each site
was represented by the cell number per unit water
volume and algal volume per unit area. Cell counts
and estimations of cell volume were conducted with
an optical microscope (Nikon E0**). The samples
were stained with *./ῌ erythrosine (*.+ mL was added
to - mL of the sample) and ultrasonicated for / minutes to loosen sedimented particles. The sample water was ﬁltered through a hydrophilized PTFE membrane ﬁlter (pore size *./ mm, +- mm diameter, Advantec, H*,*A*+-A), which became transparent with water, and the number of algae on the ﬁlter was estimated by counting the cells along a line crossing theﬁlter center (counted area/entire ﬁlter area῎..3 mm,/
12 mm,). The volume of ﬁltered water was adjusted
between /* and +*** mL to obtain an optimal cell number for the counting (/*ῌ+*** cells in the total of taxa).
The ﬁltering and counting were repeated -ῌ0 times on
the same sample until the standard error of the meanof this measurement became less than +*ῌ. Fromthe mean of the repeated measurements and the ﬁltered volume, the cell concentration (cells mLῌ+) of
the sample was obtained. Mean cell volume was estimated by the nearest geometrical approximations
using measurements of /*ῌ+** cells for each taxon(Reynolds, +32.). The total algal biomass was estimated by summing algal volume biomass of eachtaxon obtained by multiplying cell concentration by
the mean cell volume. This calculation was done foreach taxon at each site. The total biomass was represented as cell volume per unit area of glacial surface(mm- mῌ,). Community structure was represented by
the proportion of each taxon to the total algal volume.

Takeuchi et al.

Fig. +. Maps of Rikha-Samba Glacier in western Nepal
showing sites of surface snow/ice sample collection and ice core drilling. Ice core drilling was
carried out at site S1.

,.-

Ice core drilling and analysis
The ice core was drilled on a ﬂat glacial surface at
an elevation of /22* m a.s.l. above the equilibrium line
(site S1 in Fig. +). The site was located in a superimposed ice zone, where percolated melt water continuously refreezes at the interface between snow layer
and glacier ice. Superimposed ice appeared at /0 cm
below the surface at the drilling site. A +..3*-m long
ice core was recovered with a hand auger (Pico, U.S.
A.). The drilling conditions have been described by
Fujita et al. (,**,). All of the ice core sections werevertically split in half in the ﬁeld. One half of thecore was horizontally cut every / cm (total ,30 samples), melted in a clean plastic bag, and preserved inclean plastic bottles in the ﬁeld, and then transported
to a laboratory in Nagoya University, Japan. The
other half was kept frozen and transported to a coldlaboratory in the university. All of the processes inthe ﬁeld were conducted on a clean aluminum foil
spread on a box with a disposal plastic glove to avoid
contamination. Also, the surface of each piece of theice was cleaned with a ceramic knife before the ice27

was put in the plastic bag.
The samples cut in the ﬁeld were used for the
analysis of tritium, snow algae, and dust concentration. The samples for analysis of snow algae were
preserved as a -ῌ formalin solution in the ﬁeld. The
frozen core was used for a visual stratigraphy recordand density measurement in the cold laboratory. After the measurements, the core was cut every / cm
(total ,30 samples) and used for hydrogen stable isotope (dD) and soluble chemical ions analyses. Tritium concentration was measured with a liquid scintillation counter. Hydrogen stable isotope was analyzed via gas-source mass spectrometry using chrome
reduction (precision: ῎*./ῐ) in the University ofMaine. The soluble chemical ions, including ﬁve cations (Naῌ, NH.ῌ, Kῌ, Mg,ῌ, and Ca,ῌ) and seven anions(CH-COO῍, HCOO῍, Cl῍, NO,῍, NO-῍, SO.,῍, and C,O.῍),
were measured by an ion chromatography systems(Dionex DX/**). In this paper, the results of NH.ῌ,NO-῍, Ca,ῌ, and C,O.῍ are shown.
The algal biomass in the core samples was represented by the cell volume per unit volume of water.
Cell counts and estimations of cell volume were conducted with a ﬂorescence microscope (Nikon E0**).
,** mL of the sample water was ﬁltered with a hydrophilized PTFE membrane ﬁlter (the same as ﬁlter used
for surface samples), and the number of autoﬂuorescent algae on the ﬁlter was counted by thesame manner as the algal examination for the glacialsurface samples. From the mean results and ﬁlteredsample water, the cell concentration (cells mL῍+) of
each sample was obtained. The theoretical detection
limit of this analysis was *.*+῏+*/ mm- mL῍+.
Dust concentration was also quantiﬁed by microscopy using the same ﬁlter. The surface of the ﬁlter
observed microscopically was stored as a digital image ﬁle (TIFF format) on an 2-bit grey scale. Afterthe image was converted to black and white with athreshold of the maximum level of background, thenumber of particles was automatically counted with
an image-processing application (Image Pro Plus, ver.
.). Size of the dust particles by this method ranged
from / to ,** mm in diameter. The dust concentration
was obtained from the number of particles and volume of ﬁltered water. The detection limit and error
range in this procedure are /.*῏+* number mL῍+ and+*ῌ, respectively. Our method may underestimate
the dust concentration because the image processing
procedure could erase pale-colored dust particles andcould not separate overlapped dust particles on theﬁlters. The error was estimated as roughly ῍/ῌ,based on comparison of the results from this methodand direct counting with a microscope. However, thethreshold level does not a#ect the relative variation indust concentration of each sample.

Bulletin of Glaciological Research

28-.

Results-.+ Snow algal community on the glacial surface
The snow algal community on the glacial surface
consisted of mainly seven taxa (Fig. ,). Descriptionsof the seven taxa are shown in Table +.
Each taxon showed a di#erent pattern of spatial
distribution (Fig. -). C. brebissonii, Nostocaceae cyanobacterium, and Oscillatriaceae cyanobacterium ,were observed mainly in the lower part of the glacier(sites S+-S-). M. berggrenii, Chroococcaceae cyanobacterium, and Oscillatriaceae cyanobacterium + wereobserved on all of the sites from S+ to S1. The Unknown Alga was observed in mainly higher altitudes(sites S/-S1).
The total algal biomass generally decreased withincreasing altitude (Fig. .). The mean total algal biomass ranged from ..1῍+*3 to ../῍+*++ mm- mῌ, (mean:+.-῍+*++ mm- mῌ,). The largest biomass (../῍+*++ mmmῌ,) occurred at site S,. The biomass generally decreased with altitude to sites in the snow area. The
smallest biomass was found at site S0.
The community structure showed that dominantalgae di#ered among the study sites (Fig. /). In lower
sites of the glacier, Nostocaceae cyanobacterium, Oscillatriaceae cyanobacterium , and C. brébissonii were
dominant. Total biomass of the three taxa occupied
from 1* to 2*ῌ of the total at the lower three sites (STable +.

Fig. ,. Pictures of snow algae observed on Rikha-Samba
Glacier. a. Mesotaenium bregrenii; b. Unknown
Alga; c. Cylindrocystis brébissonii; d. Chroococcaceae cyanobacterium; e. Nostocaceae cyanobacterium; f. Oscillatoriaceae cyanobacterium +; g.
Oscillatoriaceae cyanobacterium ,. All pictures
were taken with a phase contrast microscope.

List of snow algae observed on Rikha-Samba Glacier and their description.

Takeuchi et al.

Fig. -. Altitudinal distribution of cell volume biomass(+*3 mm- mῌ,) of each snow alga on Rikha-Samba
Glacier. Numbers in brackets show altitude ofeach site (m a.s.l.).

Fig. .. Altitudinal change of total cell volume biomass
on Rikha-Samba Glacier.

+-S-). C. brébissonii were particularly dominant atsite S, (more than 0*ῌ of total biomass). M. berggrenii
was dominant in the middle area of the glacier (S.-S/),accounting for /*ῌ0*ῌ of the total cell volume biomass at the sites. Chroococcaceae cyanobacterium
and Oscillatriaceae cyanobacterium + were the second
and third most dominant in the middle area, respectively. In the upper area (S0-S1), Chroococcaceae cyanobacterium and Oscillatriaceae cyanobacterium +were dominant, accounting for 1*ῌ2*ῌ of the total

29

Fig. /. Altitudinal change of community structure ofsnow algae (proportion of cell volume biomass) on
Rikha-Samba Glacier. Numbers in brackets show
altitude of each site (m a.s.l.).

dominance.
-., General characteristics of ice core and results ofanalyses of stable isotope, dust, and soluble ions
The density and stratigraphy of the ice core showedthat three fourths of the core was melt and refrozen
ice (Fig. 0). The density varied from -.* to 3,+ kg mῌ(mean 0/0 kg mῌ-), and its variation in depth was
di#erent from those expected for dry-snow. Stratigraphy showed that 1/.+ῌ of the total core length
was refrozen ice. The ice layers were a mix of ice
formations with and without bubbles. Althoughsome ﬁrn layers were observed, they accounted for
only ,+.,ῌ of the total length. The remaining -.1ῌwas new snow at the glacial surface. Many visible
dust layers were observed from the surface to thebottom. Tritium analysis showed that the level was
lower than -* TU between *.* and +-.* m and there wasa signiﬁcant peak at +../ m in depth (+*+ TU, Fig. 0).
Hydrogen stable isotope varied from ῌ+.0.,῎ toῌ20.,῎ (Mean: ῌ+,*.-῎, Fig. 0). Seasonal ﬂuctuation was not clear in the proﬁle. Although some
ﬂuctuation was observed, for example, at a depth of
between / and 2 m, most of the core had little ﬂuctuation.
Microscopy revealed that the ice core contained
signiﬁcant amounts of insoluble dust particles. The
dust consisted of both mineral and organic particles.
The size of dust ranged up to +*, mm in diameter.
The proﬁle of the dust concentration showed many
spikes from the surface to the bottom of the core (Fig.
0). The concentration ranged from * to ../῍+*. particles per mL. The spikes in the dust proﬁle corre-

30

Bulletin of Glaciological Research

Fig. 0. Proﬁles of stratigraphy, density, hydrogen stable isotope (dD), dust particles, tritium, andsoluble ions (Ca,ῌ, NH-ῌ, NO-῍, C,O.῍) of the ice core of Rikha-Samba Glacier. Annual boundary
layers are indicated with the dust proﬁle.

sponded well to those of visible dust layers.
Chemical analysis showed that the core contains
various and abundant soluble ions, each of whichshowed a di#erent depth proﬁle (Fig. 0). The majorsoluble ions in this core were Ca,ῌ (2/ῌ in weight) andNH.ῌ (0ῌ) for cations, and NO-῍ (-1ῌ), SO.,῍ (,1ῌ),and Cl῍ (+2ῌ) for anions.
-.-

Snow algae in the core
Microscopy revealed algal cells in +*+ out of ,30

samples of the ice core. The algae included the fourtaxa (Fig. 1). Based on the cell size and morphologyof each taxon, they corresponded with those observedon the surface of the glacier. The taxa observed in
the ice core were Oscillatriaceae cyanobacterium +(cell size: +.-῎*., mm in diameter, mean῎SD), Oscillatriaceae cyanobacterium , (-.-῎*.- mm in diameter),Chroococcaceae cyanobacterium (..+῎+./ mm in diameter), and the Unknown Alga (+,.-῎-.. mm in diameter).

Takeuchi et al.

..
..+

Fig. 1. Photographs of snow algae observed in the icecore of Rikha-Samba Glacier. a. Oscillatoriaceae
cyanobacterium + (depth: +.-- m); b. Oscillatoriaceae
cyanobacterium , (depth: +.-- m); c. Chroococcaceae
cyanobacterium (depth: +.-- m); d. Unknown Alga
(depth: *.2- m). All photographs were taken with aﬂuorescence microscope.

Fig. 2. Proﬁles of algal cell volume biomass for total andeach taxon in the ice core of Rikha-Samba Glacier.

The total cell volume biomass of the algae in theice core varied from *.* to +3῍+*/ mm- mLῌ+ (Fig. 2).
The depth proﬁle of the biomass showed spikes.
Three remarkable spikes were observed between *..
and +.. m in depth, and the other spikes were relatively smaller. The biomass proﬁle also di#ered
among the taxa. The Chroococcaceae cyanobacterium frequently appeared from top to bottom of theice core, whereas the other three taxa rarely did so.

31

Discussion

Spatial variations in a snow algal community on theglacial surface
Most of the algae observed on this glacier corresponded to those previously reported on other Himalayan glaciers. According to the previous reports on
the other Himalayan glaciers: Yala Glacier (/+**ῌ/.**m a.s.l.) by Yoshimura et al. (+331) and AX*+* Glacier(.2**ῌ/-** m a.s.l.) by Takeuchi et al. (+332), M. berggrenii
and C. brébissonii are dominant species on the glaciers.
M. berggrenii is observed not only in the Himalayas,
but in many other cold regions in the world. Remias
et al. (,**3) have noted two variations in the cell sizeof M. berggrenii: the smaller one is M. berggrenii var.
alaskana (length: 2ῌ+0 mm, width: 2ῌ3 mm) and the larger one is a standard species (length: ,*ῌ-* mm, width:+,ῌ+- mm). The alga found on this glacier is likely thesmaller one. Oscillatriaceae cyanobacteria are also
common taxa on the ice surface of the glaciers, although it is di$cult to say that these cyanobacteria
are the same taxa based on morphological identiﬁcation. The Unknown Alga found in this study may
be Trochiscia sp. or a zygospore of a Chloromonas sp.,which are also common in the snow surface of theHimalayan glaciers (Yoshimura et al., +331; Takeuchi
et al., +332). Only the Nostocaceae cyanobacterium inthis study was not reported on the two glaciers inprevious reports.
The altitudinal change of algal biomass on theglacial surface also showed the same trend as thosereported on other Himalayan glaciers. The total cellvolume biomass decreased as elevation increased on
Yala and AX*+* Glaciers as well as on this glacier(Yoshimura et al., +331; Takeuchi et al., +332). As suggested in the previous reports, this relationship arises
from an altitudinal gradient of the surface conditions
a#ecting algal growth. In the case of the Himalayan
glaciers, availability of water and/or length of thesnow-free period are the most likely conditions a#ecting the seasonal biomass. Thus, algal biomass may
be correlated positively with the length of the surface
melting period in summer.
The community structure of snow algae also results from the change of environments on the glacialsurface. Snow algae on glaciers are usually classiﬁed
into four specialized types (e.g., Yoshimura et al., +331):
snow-environment specialists (observed on the snow
surface), ice-environment specialists (observed onbare ice), generalists (observed on both snow and ice),and opportunists (observed on a speciﬁc area of the iceor snow surface). Based on the distribution of eachspecies on this glacier and on the previous reports
showing the classiﬁcation of snow algal species on
Himalayan glaciers, M. berggrenii, Chroococcaceae cyanobacteria, and Oscillatriaceae cyanobacterium + can32

Bulletin of Glaciological Researchbe categorized as generalists, Unknown Alga as asnow-environment specialist, and C. brebissonii, Nostocaceae cyanobacterium, and Oscillatriaceae cyanobacterium , as an ice-environment specialist. The
variable conditions of the glacial surface favoring
growth of certain species are likely to result in thedi#erences in the algal community among sites.
..,

Dating of the ice core
The core was dated using records of tritium, dust
particle concentrations, and stratigraphy. Density
and stratigraphy showed signiﬁcant melt features in
the ice core. The lack of seasonal signals on hydrogen stable isotopes and chemical species is likely due
to disturbance of melt water percolation. In contrast,
there were many clear spikes in dust concentration,
which may correspond to annual layers because insoluble dust particles are less a#ected by melt waterpercolation. Many studies on ice cores have used
dust signals to date annual layers, in particular on
Asian ice cores (e.g., Thompson et al., +323; Han et al.,,**0). The dry fallout of dust particles is a common
phenomenon in this region and usually occurs in thewinter dry season (e.g., Kang et al., ,***). The e#ectof percolating water on insoluble particles in snow
has been examined in previous studies, and particles
larger than 1./ mm in diameter were less a#ected andcould stay at the original layer, whereas particles
smaller than / mm could be moved down by melt
water (Uetake et al., ,**0). Dust analyzed in thisstudy was larger than / mm and contained a signiﬁcant amount of large particles ranging up to +**mm. Thus, dust spikes in the proﬁles are likely toshow the boundaries of annual layers. Tritium records showed a maximum at a depth of +../ m, whichmost likely corresponded to the time of the atmospheric nuclear test in +30- (Fig. 0). At this depth, theyear determined by stratigraphy and dust proﬁles
was consistent with the year +30-.
The dating showed that the entire length of theice core spanned -1 years. However, since such alarge portion of the core was refrozen ice, hiatuses in
the annual layers might have occurred. Furthermore, there are some unclear small dust peaks, whichmight cause misreading of the annual boundary.
Thus, the dating possibly includes an error of + or ,years.
..-

Temporal variations in snow algae derived from theice core
The annual variation in the total algal biomass ofthe snow algae showed that the biomass was high in+30/ῌ01, +311, +32+, +320, and +33,ῌ32, and it reachedparticularly high levels in the late +33*s (Fig. 3). The
biomass in +33*, +322, +32*, +31-, and +30, was under thedetection level. The total annual biomass varied from*.* to 30῎+*3 mm- m῍, a῍+ (mean, ...῎+*3 mm- m῍, a῍+).

Fig. 3. Annual variations in algal volume biomass, massbalance, dust ﬂux, soluble ions (total nitrogen, NH.ῌ,NO-῍, Ca,ῌ, C,O.῍), and hydrogen stable isotope (dD),for -1 years derived from the ice core of RikhaSamba Glacier.

Fig. +*. Di#erence in community structure of snow
algae in speciﬁc years derived from ice core of RikhaSamba Glacier. Community structures shown here
are from years in which the algal biomass washigher than , ῎ +*3 mm- m῍, a῍+.

The increase in the +33*s was particularly signiﬁcant:the mean biomass in the +33*s was almost +0-foldgreater than that before +33* (+1῎+*3 versus +.+῎+*3
mm- m῍, a῍+).

Takeuchi et al.

The variation in snow algal biomass in the icecore may indicate di#erences of algal growth in eachyear; however, there are many other possible factorsthat might a#ect the algal biomass in the ice core.
One of them is spatial variation in algal biomass on
the glacial surface. According to the surface algal
biomass examined in this study, the standard deviation of the spatial biomass variation averaged /./῍+*3
mm- mῌ, in the upper snow area (sites S0 and S1). The
range of the annual biomass before the +33*s (*.* m -.3
῍+*3 mm- mῌ, aῌ+) was smaller than the standard deviation, so spatial variation cannot be excluded fromthe possible factors a#ecting the biomass before the+33*s. However, the mean biomass in the +33*s (+1῍+*3 mm- mῌ, aῌ+) signiﬁcantly exceeded the standard
deviation. Therefore, the biomass increase in the+33*s is unlikely to be due to spatial variation, but
probably reﬂects the algal growth on the glacial surface during that period of time.
The biomass variation could also be a#ected bydecomposition after the algae were buried in the glacial snow and/or ice. Yoshimura et al. (,**0) haveshown the variation of snow algal biomass in a 1 m
deep ice core on the Yala Glacier (/-/* m a.s.l.) in the
Himalayas, and have mentioned that algal cells are
possibly decomposed by autolysis or bacterial decomposition in layers deeper than / m. The Yala Glacieris a temperate glacier: the temperature of all glacial
ice is near the melting point (between ῌ+ and *῎from the surface to 0* m depth; Watanabe et al., +32.).
This higher ice temperature may allow the diagenesisof algal cells in the deeper part of the glacier. In
contrast, the Rikha-Samba Glacier in this study is acold continental-type glacier; the ice temperature in
the accumulation zone ranged from ῌ1 to ῌ.῎ between the surface and ,-.,/ m deep (Fujita et al., +331;
Fujii et al., +330). Therefore, algae in the ice core ofthis glacier could be preserved better than that of theYala Glacier.
The ice core record showed that the species composition of snow algae also varied annually. Figure+* shows the species composition of snow algae in theyears in which the algal biomass was higher than ,῍ +*3 mm- mῌ, aῌ+. The two algae, Oscillatriaceae cyanobacterium + and Chroococcaceae cyanobacterium,
appeared in all of the years, whereas the other two
taxa in only certain years. The common two taxa
were the dominant species in the upper part of theglacier in the altitudinal distribution (Fig. /). This
di#erence in algal community structure is likely toresult from variation in the algal community growneach year. Although spatial variation in algal community may also result in the di#erence among theannual layer, the results of examination of the surface
algal community showed that species composition
was spatially uniform over the surface. On the basisof the species composition, the communities can be

33

classiﬁed into three types: Type + is a community consisting of two species: Oscillatriaceae cyanobacterium+ and Chroococcaceae cyanobacterium (+30., +33-, +33/).
Type , is a community consisting of three species, twoof Type + and Unknown Alga (+320, +331, +332), while
Type - is a community including Oscillatriaceae cyanobacterium , (+300, +330).
These signiﬁcant annual variations in algal communities could be further explained by the shift in thealtitudinal distribution of snow algae on the glacialsurface. For example, the large biomass in +330 (30῍+*3 mm- mῌ, aῌ+) is equivalent to that on the glacialsurface between /0** and /1** m a.s.l. (Fig. .). Thissuggests that the surface conditions at the drilling sitein +330 were similar to those on the glacial surface ,**ῌ-** m lower than the drilling site. Thus, the algal
distribution on the glacial surface in +330 may haveshifted ,**--** m upward. The community structure
observed in each annual layer in the core also corresponded to that observed on the glacial surface. The
algal community in +330 and +300 was Type -, which
included an alga of Oscillatriaceae cyanobacterium ,.
This alga was an ice-environment specialist, observedin the middle to lower part of the glacial surface (Fig.
/). Thus, the surface conditions of the drilling site in+330 and +320 might be similar to the ice surface in the
middle to lower part of the glacier in +332. The algal
community in +320 and +331 was a Type , community,
which is of the same species composition as at thesurface of the drilling site in +332 (Fig. +*). Thus, thesurface conditions in +320 and +331 appeared to be
similar to those in +332. The surface conditions in
the years of smaller or no algal biomass are likely notsuitable for algal growth. Such conditions might correspond to a surface at an elevation higher than the
drilling site. Thus, the variation in algal community
in the ice core suggests that altitudinal distribution ofsnow algal communities could shift up or down on theglacial surface from year to year. The shift may
depend on the physical or chemical conditions on theglacial surface in each season.
The algae found in the ice core were only four outof the seven taxa observed on the glacial surface.
The other three algae may not grow at the top of theglacier during that period of time or readily decomposed in the ice. M. berggrenii, which was the dominant species in the middle part of the glacier (Fig. /),was not found in the ice core, although the other algaein the middle to lower part of the glacier were observed. M. berggrenii may be decomposed or destroyed easier than the other species...

Comparison of algal variations to mass balance,
dust, and soluble ions in the ice core
The physical and chemical conditions that a#ect
annual growth of snow algae on the glacier may berecorded in the ice core. One of the possible factors

34

Bulletin of Glaciological Researcha#ecting the algal community on the surface is net
mass balance (net accumulation) of the glacier. Annual net mass balance of the glacial surface generally
increases as altitude increases, and also depends on
the amounts of accumulation and ablation. Intensive
ablation in summer possibly causes more algal growth
because algal growth requires liquid melt water. Our
previous study showed that altitudinal variation in analgal community on the glacial surface corresponded
well to the surface mass balance (Takeuchi et al.,+332). As compared with mass balances obtained
from the annual layers of the ice core, however, thealgal biomass was not correlated with the mass balance (Fig. 3).
The melting history of Himalayan glaciers (+30/ῌ+330) has been extracted by Fujita et al. (,**0) basedon two net balance records of glaciers located approximately ,** km east of the Rikha-Samba Glacier.
Their results showed that glacial melting increased
during +303ῌ1+, +32*ῌ2+, and +33*ῌ3,. Snow algae canbe expected to grow intensely in these periods. However, these periods do not coincide with the years ofhigh algal biomass in the ice core. Furthermore,
there is no similarity between variations in the algal
community and air temperatures of Kathmandu (thecapital of Nepal, /** km east of the glacier) and the /**hPa NCEP/NCAR reanalysis data of Fujita et al.
(,**0). Stable isotopes in the ice cores could also be
indicative of climate conditions each year since theyusually reﬂect regional air temperatures and also
monsoon activity (e.g., Thompson et al., ,***). However, hydrogen stable isotopes in most of this ice core
seem to be modiﬁed by melt water percolation andruno#, so they can not be used as a climate signal.
The dust concentration is also a possible factor in
the temporal variations in the snow algal community,
since dust contains algal spores and also provides themain nutrient source for algal growth on the glacialsurface (Yoshimura et al., +331; Marshall and Chalmers,+331). The variations in dust ﬂux peaked in the mid+30*s and mid-+33*s (Fig. 3). These dust peaks coincide with the years in which algal biomass was highand the Type - algal community appeared. Suchsimilarities suggest that the annual variations insnow algae were a#ected by the ﬂux of the windblown dust. However, since the peak of dust ﬂux inthe +33*s was comparable to the peak in the +30*s, thesigniﬁcant increase in biomass during the +33*s can
not be explained by dust ﬂux variations alone.
Compared with concentrations of soluble ions in
the ice core, the emergence of the algal community did
not appear to coincide with most ions. Total soluble
nitrogen (NH.ῌ, NO-῍, and NO,῍), which is derived
from biogenic or agricultural sources in lower parts ofthe valleys (Shresta et al., +331), is expected to a#ect
algae since it can serve as a nutrient for them. The
variations in NH.ῌ, NO-῍, and NO,῍ showed di#erent

trends, and total nitrogen increased in the early +32*s
and +33*s (Fig. 3). However, the variation did notagree with that of algal biomass. The temporal variations in carboxylic acids (formate, acetate, and oxalate; only oxalate is shown in Fig. 3) showed an increasing trend in the +30*s and +33*s, which coincidedwith an increase of algal biomass. However, the variation in carboxylic acids is unlikely to cause the algal
variation because the carboxylic acids do not appear
to be derived from sources other than the glacier, butrather from biological activity on the glacial surface.
Although our results could not deﬁnitively demonstrate the factors a#ecting algae, variation in thealgal community may be due to the combination ofsome physical and chemical factors. In particular,
the signiﬁcant increase in algal biomass during the+33*s is likely due to the recent changes in glacial
environments so often reported in this region. Glacial shrinkage and climate warming have recently
been reported in the Himalayan region. Massbalance studies in the Himalayas have shown thatglacial shrinkage was particularly signiﬁcant in the+33*s (Fujita et al., ,**+a, ,**+b). Recent increases inoxygen- or hydrogen-stable isotopes are commonly
observed in many ice cores from Asian glaciers, suggesting recent climate warming (e.g., Thompson et al.,+323, +33-, ,***). Both the shrinkage of glaciers andclimate warming indicate that the melting intensityof glacial surfaces has recently increased. Such changes
can increase liquid water availability on the glacialsurface and extend the growth period of snow algae.
Furthermore, dramatic increases of soluble ions suchas ammonia since the +3/*s have been reported on
glacial snow in the Himalayan region due to anthropogenic emissions from enhanced agricultural activities and energy consumption over Asia (e.g., Kang etal., ,**,). These changes could make the surface conditions more favorable to the growth of algae.
It should be noted that the discussion on algal
variation in the ice core is based on the assumptionthat diagenesis of algal cells did not occur in theglacial ice. Although the physical conditions at thedrilling site could support this assumption as mentioned previously, there is no direct evidence. Morestudies on the diagenetic process of snow algae inglacial ice are warranted. Otherwise, genetic and/or
carbon and nitrogen stable isotope analyses on thebiogenic material in glacial ice would be more usefulto study paleo-ecology on glaciers, since these results
are less inﬂuenced by diagenesis. However, there islittle information about genetic and carbon/nitrogenstable isotopes of glacial organisms on Himalayan
glaciers, so further basic studies are required.

Acknowledgments
We wish to thank the sta# of the Department of

Takeuchi et al.

Hydrology and Meteorology, Government of Nepal
and the members of the CREH project for supporting
our ﬁeldwork. We are also indebted to Dr. Karl Kreutz
for his stable isotope analysis, Drs. Yoshiyuki Fujii
and Makoto Igarashi for their tritium analysis, Mr.
Toshiaki Miyajima for his assistance with the microscopy analysis, and anonymous reviewers for valuablesuggestions, which signiﬁcantly improved this manuscript. The ﬁeldwork was supported by a Grant-inAid for scientiﬁc research (No. ,+02+**-, +3-+**,*,*3.3**+2), and the laboratory work by the research
project “Ice core analysis with cryo-microbes on glaciers in an arid Chinese region,” supported by theSpecial Coordination Funds for Promoting Scienceand Technology from the Japanese Ministry of Education, Culture, Sports, Science and Technology, andby the research project.

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