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Distribution and phylogeny of Glacier ice worms (Mesenchytraeus solifugus and Mesenchytraeus solifugus rainierensis)


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Glacier ice worms, Mesenchytraeus solifugus (Emery, 1898) and Mesenchytraeus solifugus rainierensis Welch, 1916 (Enchytraeidae), are the only known oligochaetes adapted to life in ice. We have collected ice worm specimens from over 100 populations throughout the Pacific northwestern region of North America. Their current range extends ~2500 km along the Pacific coastline between south-central Alaska and central Oregon, with most populations occurring on relatively low-elevation, temperate glaciers. Phylogenetic analyses utilizing partial nuclear 28S rDNA and mitochondrial cytochrome c oxidase subunit I (COI) loci revealed the presence of two geographically distinct clades (northern and southern). The northern clade comprises all Alaskan populations, while the southern clade contains British Columbia, Washington State, and Oregon State populations. No evidence of gene flow was detected between these two lineages or between noncontiguous glaciers throughout their geographic range. Our results suggest that the mechanism of ice worm dispersal is primarily active, though at least one episode of passive dispersal is noted at the southern extent of their range.
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Distribution and phylogeny of glacier ice worms
(Mesenchytraeus solifugus and Mesenchytraeus
solifugus rainierensis)
Paula L. Hartzell, Jefferson V. Nghiem, Kristina J. Richio, and Daniel H. Shain
Abstract: Glacier ice worms, Mesenchytraeus solifugus (Emery, 1898) and Mesenchytraeus solifugus rainierensis
Welch, 1916 (Enchytraeidae), are the only known oligochaetes adapted to life in ice. We have collected ice worm spec-
imens from over 100 populations throughout the Pacific northwestern region of North America. Their current range ex-
tends ~2500 km along the Pacific coastline between south-central Alaska and central Oregon, with most populations
occurring on relatively low-elevation, temperate glaciers. Phylogenetic analyses utilizing partial nuclear 28S rDNA and
mitochondrial cytochrome coxidase subunit I (COI) loci revealed the presence of two geographically distinct clades
(northern and southern). The northern clade comprises all Alaskan populations, while the southern clade contains Brit-
ish Columbia, Washington State, and Oregon State populations. No evidence of gene flow was detected between these
two lineages or between noncontiguous glaciers throughout their geographic range. Our results suggest that the mecha-
nism of ice worm dispersal is primarily active, though at least one episode of passive dispersal is noted at the southern
extent of their range.
Résumé : Les vers de glaciers, Mesenchytraeus solifugus (Emery, 1898) et Mesenchytraeus solifugus rainierensis
Welch, 1916 (Enchytraeidae), sont les seuls oligochètes connus adaptés à la vie dans la glace. Nous avons récolté des
spécimens de vers de glaciers dans plus de 100 populations dans toute la région pacifique du nord-ouest de l’Amérique
du Nord. Leur répartition actuelle couvre ~2500 km le long de la côte du Pacifique, du centre-sud de l’Alaska au
centre de l’Oregon, la plupart des populations se retrouvant sur des glaciers tempérés d’altitude relativement basse. Des
analyses phylogénétiques basées sur le séquençage partiel des locus de l’ADNr 28S nucléaire et de la sous-unité I de
la cytochrome coxydase (COI) mitochondriale révèlent l’existence de deux clades distincts (boréal et austral). Le clade
boréal regroupe toutes les populations de l’Alaska, alors que le clade austral contient les populations de Colombie-
Britannique et des états de Washington et d’Oregon. Nous ne décelons aucune indication de flux génétique entre ces
deux lignées, ni entre les populations de glaciers non contigus dans l’ensemble de l’aire de répartition. Nos résultats
laissent croire que les mécanismes de dispersion des vers de glaciers sont surtout de type actif; il a cependant un cas
de dispersion passive à signaler à l’extrême sud de leur aire de répartition.
[Traduit par la Rédaction] Hartzell et al. 1213
Glaciers are among the least explored ecosystems, yet
they hold about 75% of the world’s freshwater supply and
cover approximately 10% of the Earth’s land surface. Gla-
cier ice worms, Mesenchytraeus solifugus (Emery, 1898) and
Mesenchytraeus solifugus rainierensis Welch, 1916, are the
only known oligochaetes adapted to life in glacier ice. Their
unusual habitat makes them a species of evolutionary inter-
est, yet they have not been included in prior phylogenetic
studies of Enchytraeidae, and are poorly represented in pub-
lished studies on Clitellata.
The species was first described by Emery (1898a, 1898b,
1898c, 1900) based on specimens collected from Malaspina
Glacier, Mount St. Elias, Alaska. Moore (1899) corrected
Emery’s designation from Melanenchytraeus to the pre-
existing Mesenchytraeus genus. Welch (1916a, 1916b,
1917a), Goodman and Parrish (1971), and Shain et al.
(2000) further described their morphology, and to a lesser
extent, their ecology. Glacier ice worms have been docu-
mented from some glaciers in Alaska (Emery 1898a, 1898b;
Moore 1899; Eisen 1905; Odell 1949; Tynen 1970; Russell
1892; Shain et al. 2001), British Columbia (Welch 1917a;
Tynen 1970), and Washington State (Welch 1916a, 1916b;
Gudger 1923; Tynen 1970). Welch (1916a, 1916b) proposed
the subspecies Mesenchytraeus solifugus rainierensis based
on morphological differences between Mt. Rainier, Wash-
ington, ice worms and Alaskan glacier ice worms (e.g.,
smaller number of setae per bundle, only two instead of
three diverticula on the spermathecae, straighter speriducal
Can. J. Zool. 83: 1206–1213 (2005) doi: 10.1139/Z05-116 © 2005 NRC Canada
Received 29 December 2004. Accepted 15 August 2005. Published on the NRC Research Press Web site at on
22 September 2005.
P. Hartzell1and K.J. Richio. Clark University, Department of Biology, 950 Main Street, Worcester, MA 01610, USA.
J.V. Nghiem1and D.H. Shain.2Rutgers The State University of New Jersey, Department of Biology, 315 Penn Street, Camden,
NJ 08102, USA.
1Equally contributing authors.
2Corresponding author (e-mail:
funnel, complete enclosure of the sperm sacs and ducts by
the ovisac). Hartzell (2005) noted significant differences in
the mean sizes of Washington State (~1.5 cm long, ~300 µm
wide) versus Alaskan (~1 cm long, ~250 µm wide) ice worms.
Dietary information is limited to cursory examinations of
gut contents, and suggests that ice worms ingest glacial al-
gae and other organic debris found in ice and snow (Emery
1900; Goodman 1971). Ice worms are highly pigmented
compared with other enchytraeids, presumably an adaptation
related to elevated levels of radiation in a glacial environ-
ment (Emery 1898a, 1898b, 1898c, 1900; Moore 1899;
Welch 1916a, 1916b, 1917a; Goodman and Parrish 1971).
Ice worms otherwise display no apparent morphological
adaptations to their extreme environment (Goodman and
Parrish 1971; Shain et al. 2000). While other enchytraeids
endure Arctic permafrost by dehydration (Holmstrup and
Westh 1994; Sømme and Birkemoe 1997; Pedersen and
Holmstrup 2003) or by accumulating sugars (Holmstrup and
Sjursen 2001; Holmstrup et al. 2002), these mechanisms do
not appear useful to ice worms that survive in a hydrologic
environment which vacillates only a few degrees from 0 °C.
Recent biochemical analyses indicate that ice worm
adenylate levels (e.g., ATP) are unexpectedly high and con-
tinue to rise as temperatures fall, suggesting a compensatory
adaptation in ice worm energy metabolism (Napolitano and
Shain 2004; Napolitano et al. 2004).
The purposes of this study were to establish the current
geographic range of glacier ice worms and to identify any
large-scale evolutionary relationships between populations
based on molecular data. Our analyses indicate that ice
worms form distinct northern and southern clades, and that
most populations appear to be genetically isolated.
Materials and methods
Field methods
In total, 145 glaciers were included in this study. Of these,
49 glaciers were subject to systematic survey along one or
more longitudinal transects, beginning as close to the glacier
terminus as possible and continuing up-glacier as high as
possible given safety considerations. Data and sample col-
lection stations were placed every 50- to 100-m intervals
along a transect, depending on the size of the glacier (e.g.,
on glaciers <300 m in length, sampling intervals were short-
ened to 50 m to have multiple samples on a transect, but
transects were typically >500 m in length). Collections were
made between May and August during the 2000–2004 field
seasons. Ice worms were collected after sundown and before
sunrise, when they appear on the glacial surface (Goodman
1971; Tynen 1970; Shain et al. 2001). Population densities
were estimated as described (Shain et al. 2001); briefly, ice
worms were counted in square-metre plots at collection sta-
tions and averaged along each transect. Field sites were in
Alaska, California, Montana, Oregon, and Washington in the
United States, and Alberta and British Columbia in Canada.
A complete list of survey sites is available (Table S1)3.
Additional ice worm specimens were provided by Begich
Boggs Visitor’s Center, Chugach National Forest, Alaska;
Roberta Holden and Sheila Byers (Vancouver Natural
History Society, British Columbia); and Heidi Weigner
(University of Alaska, Anchorage). Specimens of
Mesenchytraeus pedatus Eisen, 1905 were provided by
Steve Fend (USGS Water Resources); Mesenchytraeus
gelidus Welch, 1916 (Yosemite snow worms) by Kathryn
Coates (Bermuda Biological Research Station); and
Mesenchytraeus flavus and Mesenchytraeus armatus
Levinson, 1883 by Tarmo Timm (Estonian Agricultural Uni-
versity, Tartu).
Molecular methods
Live ice worms were either placed in 95% ethanol in the
field or packed in snow and expressed-mailed to one of our
home institutions. Ethanol-preserved specimens were selected
randomly from each population (usually from multiple col-
lection stations along a transect to represent different
microhabitats; e.g., snow, firn, crevasse pools, ice) and
rehydrated before DNA extraction. Genomic DNA from
individual worms was extracted by standard phenol–
chloroform methods (Lee and Taylor 1990), or by an Omega
E.Z.N.A. forensic DNA kit. A 731 base pair (bp) fragment
from the 5end of nuclear 28S rDNA was amplified by the
polymerase chain reaction (PCR) with primers LROR (ACC-
CG). PCR conditions were as follows: 94 °C for 30 s, 50 °C
for 30 s, 72 °C for 1 min (40 cycles), and 72 °C for 10 min.
A 493-bp fragment from the 5end of mitochondrial cyto-
chrome coxidase subunit I (COI) was amplified with prim-
(CTACGTTGGGCTGCGAATC). PCR conditions were as
follows: 94 °C for 15 s, 51 °C for 1 min, 72 °C for 1 min
(35 cycles), and 72 °C for 10 min. The 28S rDNA and COI
analyses were conducted independently in different laborato-
ries, and therefore these loci were generally not sequenced
in the same individual.
PCR products were purified using a Q-Biogene BIO 101
GeneClean kit. Sequencing reactions for 28S rDNA were
performed using the following primers: LROR, LR5, LR3
an ABI 377-XL automated sequencer. COI primers (above)
were used for sequencing as above or by Northwoods DNA
(Becida, Minnesota).
Other 28S rDNA and COI sequences were obtained from
NCBI GenBank. Lists of sequences included in this study
are listed in Table 1 (28S) and Table 2 (COI). Nucleotide se-
quences were aligned in Clustal X (Thompson et al. 1997),
with manual adjustments made in McClade version 4.06
(Maddison and Maddison 2004) or BioEdit (Hall 1999).
Phylogenetic analysis
Optimal model parameters were chosen by model testing
on the ice worm data set with ModelTest version 3.06
(Posada and Crandall 1998) using 10 rate classes and α=
0.01. For the 28S sequences, optimal parameters based on
Akaike’s Information Criterion (AIC) model testing were
general time reversible plus gamma nucleotide substitution
© 2005 NRC Canada
Hartzell et al. 1207
3Table S1 containing supplementary data for this article is available on the Web site or may be purchased from the Depository of Unpub-
lished Data, Document Delivery, CISTI, National Research Council Canada, Building M-55, 1200 Montreal Road, Ottawa, ON K1A 0R6,
Canada. DUD 4022. For more information on obtaining material refer to
(GTR + Γ), with a log likelihood of –6809. Optimal parame-
ters based on hierarchical model testing were Tamura–Nei
two parameter plus gamma (TrN + Γ), with a log likelihood
of –6821. (For a discussion of the advantages and disadvan-
tages of different model testing see Posada and Buckley
2004). Trees based on GTR + Γand TrN +Γwere not nota-
bly different; the final analyses were based on GTR + Γpa-
rameters. For COI sequences, both hierarchical and AIC
model testing identified general time reversible plus gamma
plus codon (GTR + Γ+ I) as most optimal, with log-
likelihood scores of –12 292.
Each locus was analyzed separately, as there were insuffi-
cient numbers of sequences from the same specimen at both
loci to allow the two data sets to be joined. A freshwater
leech, (Haemadipsidae; AY101558) was used to root the fi-
nal 731-bp 28S alignment. The 493-bp alignment of COI se-
quences was rooted using a Lumbriculus variegatus Mueller,
1774 sequence (AY519464) as the outgroup. Bayesian anal-
ysis (BA) was performed for 10 million replicates, with a
burn-in of 10 000 trees and tree sampling every 1000 gener-
ations, using MrBayes version 3.0B4 (Huelsenbeck and
Ronquist 2003). Phylogenetic trees were generated under
maximum likelihood (ML) criterion using TreeFinder (Jobb
et al. 2004). ML analysis used general time reversible plus
gamma plus codon (GTR + Γ+ I) as most optimal, 4 rate
categories, 50% consensus, and a population size of 4, for
10 000 replicates for each locus. Branch support was as-
sessed through posterior probabilities for BA, and with boot-
strapping for ML.
Type specimens
The location of the holotypes for M. solifugus and M. s.
rainierensis is unknown to the best of our knowledge. Origi-
nal paratypes are stored at the United States Natural History
Museum. Paratypes from our work are stored with Mount
Rainier National Park, Ashford, Washington, and the Royal
British Columbia Museum, Vancouver.
Glacier ice worm distribution
To date, ice worm populations have been confirmed on
106 different glaciers in the Pacific northwest of North
America (Fig. 1; a full list is also available from Table S13).
It is noteworthy that ice worms were not found on all gla-
ciers within this range nor as far inland as the Rocky Moun-
Ice worm densities within populations (i.e., in square-
metre plots) were generally lower in the northern half of
their geographic range. For example, mean densities on
Alaskan glaciers seldom exceeded 100/m2, but were
>400/m2in the Pacific, North Cascades, and Olympic
ranges. Ice worms were found on some glaciers in the Kenai
Peninsula of south-central Alaska (e.g., Alice, Exit, Por-
tage), but they were not found on the Matanuska Glacier just
to the east in the Chugach Mountains (which lies ~50-km in-
land), nor were they found on glaciers in the Valdez, Alaska,
area. In southeastern Alaska, ice worms were not found in
the Juneau Icefield (northern Coastal Range); however, they
are present farther north, in the Glacier Bay region (Tynen
1970; Goodman 1971), and on coastal glaciers of the Alsek
Range (e.g., Grand Pacific, Grand Plateau, and Ferris gla-
ciers). Ice worms have not been observed above an elevation
of ~1400 m in this area (R. Holden, personal communica-
tion) and were generally below 1000 m on Alaskan glaciers.
© 2005 NRC Canada
1208 Can. J. Zool. Vol. 83, 2005
Family and species Location GenBank accession No. Source
Mesenchytraeus pedatus California DQ164256, DQ164257 S. Fend, personal
Mesenchytraeus solifugus Alaska, British Columbia,
Oregon, Washington AY613868, AY577788–AY577802,
Lumbriculus variegatus AY519464 D.A. Price and M.E.
Table 2. Cytochrome coxidase subunit I (COI) sequences.
Family and species Location GenBank accession No. Source
Achaeta bohemica AF406595 Jamieson et al. 2002
Enchytraeus albidus AF406597 Jamieson et al. 2002
Fredericia bisetosa AF406596 Jamieson et al. 2002
Mesenchytraeus armatus Estonia DQ164254 T. Timm, personal communication
Mesenchytraeus flavus Estonia DQ164255 T. Timm, personal communication
Mesenchytraeus gelidus California DQ164250–DQ164253 K. Coates, personal communication
Mesenchytraeus solifugus Alaska, British Columbia,
Oregon, Washington AY227193, AY303941–AY303947,
Freshwater leech AY101558 Jamieson et al. 2002
Table 1. Large subunit ribosomal RNA (28S) sequences.
By comparison, in the southern part of their distribution
(i.e., southern British Columbia, Washington, and central
Oregon), ice worms were present on nearly all glaciers that
were explored (generally an elevation <2500 m). Indeed, in
the Pacific, North Cascades, and Olympic ranges, only ice
remnants were recorded as having no or low densities of ice
worms. All 51 active glaciers surveyed in this subregion had
moderate to high densities (400–1000/km2) of ice worms
across their surfaces during late-evening hours in summer
(i.e., after sundown and before sunrise). The absence or low-
density counts exhibited on nonactive ice remnants (n=3)
in this subregion suggests some role in glacial activity for
supporting ice worm populations.
One notable gap in ice worm distribution in the southern
part of their range is on Mt. Hood, Oregon, where no ice
worms were found, even though this mountain lies between
areas that support large ice worm populations (e.g., Mt.
Rainier, Mt. St. Helens before eruption, Mt. Jefferson, the
Sisters). The apparent absence of ice worms on Mt. Hood
was confirmed by local climbers and forest managers. Ice
worms were not found on glaciers in the Rocky Mountain
regions of Canada or the United States, or south of the Sis-
ters Range in Oregon.
The 80% majority rule tree from BA of 28S rRNA and
COI sequences are presented in Figs. 2 and 3, respectively;
the single most likely trees from the ML analysis of each
loci were nearly identical (data not shown). As expected, the
Yosemite snow worm (M. gelidus) branched off most
closely to the ice worm clades, preceded by an earlier split
of M. armatus and M. flavus. Thus, the genus Mesenchy-
traeus appears to be phylogenetically supported within the
limits presented in this analysis.
Two distinct clades (i.e., northern and southern) were
formed by ice worm sequences on the COI tree (Fig. 3)
where greater variation in sequences allowed better resolu-
tion at shallower nodes. The level of sequence divergence
between the two clades was ~2% for 28S rRNA and ~10%
for COI. The node representing the bifurcation of the north-
ern and southern regions had strong support in the BA and
ML analyses. The northern clade includes all the Alaskan
ice worm sequences from this study. Sequences obtained
from the St. Elias area appear the most basal and variable
than those from any other northern subregion. Those from
the Kenai area in Alaska (e.g., Exit, Marathon) appear more
derived, suggesting ice worm expansion to this area through
a founding population (Ibrahim et al. 1996).
The southern clade comprises all British Columbia, Wash-
ington, and Oregon ice worm sequences. Those from the
southern-most part of this clade’s range, namely those from
Oregon, Mount Rainier, and the Glacier Peak/Daniels area,
formed distinct subclades within the larger clade, respec-
tively. Those from the Pacific Range/North Cascades of Brit-
ish Columbia and northern Washington State were much
more variable, suggesting that the greatest genetic diversity
is centered in the northern part of this clade’s range. Surpris-
ingly, gene flow was not apparent between ice worm popula-
© 2005 NRC Canada
Hartzell et al. 1209
Fig. 1. Distribution of glacier ice worms (Mesenchytraeus solifugus and Mesenchytraeus solifugus rainierensis). Representation of loca-
tions is approximate. Open circles indicate sites where ice worms have been confirmed; solid squares indicate sites visited, but where
no ice worms were found. Shaded areas indicate regions with current glaciation. Ice worms were found on an ~2500-km strip along
the Pacific coastline between south-central Alaska and central Oregon, predominantly on low-elevation, temperate glaciers.
tions on noncontiguous ice throughout their geographic
range (as evidenced by the absence of shared 28S rRNA or
COI genotypes).
Tynen (1970) reported that ice worms occur in coastal
glaciers from Bagley Icefield in Alaska to Mt. Rainier in
Washington State, and hypothesized that extant ice worm
populations were likely remnants of a pan-Cordilleran popu-
lation. During the course of this study, however, we have
recorded ice worms in central Oregon, well outside the max-
imum extent of the Cordilleran ice sheet (e.g., Porter and
Denton 1967; Waitt and Thorson 1983). The Oregon ice
worm populations may have originated from an earlier, pre-
Cordilleran ice age, or perhaps a founding population dis-
persed passively via aviary transport (e.g., Edwards and
Bohlen 1996; Milbrink 20034). The very limited variability
of Oregon sequences seems to support the latter hypothesis.
The clear discontinuity of the northern versus southern
clades, and the lack of ice worms on many glaciers in the
northern half of their geographic range, however, suggests
that ice worms lack a robust dispersal mechanism. The ap-
parent lack of ice worms on Mt. Hood, with substantial ice
© 2005 NRC Canada
1210 Can. J. Zool. Vol. 83, 2005
Hirudinida: freshwater leech (outgroup)
Enchytraeidae: Achaeta bohemica
Enchytraeidae: Fredericia bisetosa
Enchytraeidae: Enchytraeus albidus
Enchytraeidae: Mesenchytraeus armatus
Enchytraeidae: Mesenchytraeus flavus
Enchytraeidae: Mesenchytraeus gelidus
Enchytraeidae: Mesenchytraeus gelidus
Enchytraeidae: Mesenchytraeus gelidus
Enchytraeidae: Mesenchytraeus gelidus
Alaska: Grand Pacific
Alaska: Grand Pacific/Junction
Alaska: Grand Pacific/Junction
Alaska: Grand Pacific/Junction
Alaska: Byron
Alaska: Portage
Washington: Williwakas
Washington: Williwakas
Washington: Rainbow
Washington: Easton
Washington: Easton
Washington: Baker
Washington: Daniels
Washington: Ice Worm
Washington: Whiteriver
Washington: Whitechuck
Washington: Honeycomb
St. Elias
Glacier Peak/
Daniels Area
Ice Worms
Fig. 2. Majority rule consensus tree of glacier ice worms based on Bayesian analysis of nuclear 28S ribosomal RNA (731 base pair
partial fragment). Numerical values >50 are indicated and represent posterior probabilities. Scale indicates number of substitutions per site.
4G. Milbrink. 2003. Distributional patterns of freshwater tubificid oligochaetes and the capacities for long-way dispersal of tubificids and
other freshwater invertebrates with particular reference to “alien” species and birds as vectors of dispersal. In Proceedings of the 9th Interna-
tional Symposium on Aquatic Oligochaeta, Wageningen, the Netherlands, 6–10 October 2003. Edited by P.F.M. Verdonschot. Submitted for
worm populations 125 km to the north and 80 km to the
south, highlights this isolation. This gap in ice worm distri-
bution in the southern region is perhaps due to a stochastic
event (i.e., local extinction); their absence on all four of the
Mt. Hood glaciers surveyed suggests that such an event
probably preceded the separation of these glaciers. Mt. Hood
erupted in the 1790s, and again in the mid-1800s (Gardner et
al. 2000), raising the possibility that either or both of these
eruptions are related to the current absence of ice worms at
this location. It is also possible that Mt. Hood’s glaciers
© 2005 NRC Canada
Hartzell et al. 1211
(Lost Provenience)
El Dorado
Overlord Black Fin
Black Fin
Black Fin
Black Fin
Black Fin
Black Fin
Paradise Paradise
Wedgemount Disconnect
Paradise Disconnect
Paradise Disconnect
Paradise Disconnect
El Dorado
El Dorado
Wedgemount Disconnect
El Dorado
Wedgemount Disconnect
Enchytraeidae: Mesenchytraeus pedatus
Enchytraeidae: Mesenchytraeus pedatus
Milk Learnard
Exit Exit
Grand Pacific/Junction
Grand Pacific/Junction
Grand Pacific
Grand Pacific
St. Elias
Pacific Range/
North Cascades
Glacier Peak/
Daniels Area
Mount Rainier
British Columbia, Oregon and Washington
Glacier Ice Worms
83 100
73 64
Lumbriculidae: Lumbriculus variegatus
Fig. 3. Strict consensus tree of glacier ice worms based on Bayesian analysis of mitochondrial cytochrome coxidase subunit 1 (COI;
493 base pair partial fragment). Pacific Range / North Cascades Range leaves are indicated by double lines. Numerical values >50 are
indicated and represent posterior probabilities. Scale indicates number of substitutions per site.
were never colonized, and that colonization of Mt. Jefferson
and glaciers of the Sisters Range to the south represent sepa-
rate, independent events. The apparent absence of ice worms
on inland glaciers of Alaska and the Rocky Mountain region
may be due to severe climate regimes where biota must sur-
vive temperatures well below –5 °C. Note that ice worm
protoplasm freezes at –6.8 °C (Edwards 1986).
The lack of detectable gene flow between noncontiguous
glaciers throughout their geographic range further suggests
that ice worms lack a robust dispersal mechanism. With the
exception of the Oregon populations (e.g., Mt. Jefferson, the
Sisters), ice worm dispersal has probably been active
throughout most of their range. Thus, ice worms likely ex-
pand their range during periods of glacial maxima, in con-
trast with most temperate species that disperse rapidly during
interglacial periods following episodes of refugia (Hewitt
2000, 2004).
Phylogenetic evidence presented in this report supports
the monophyletic status of the glacier ice worm, with the ca-
veat that few Mesenchytraeus species have been collected.
The only other morphologically and ecologically compara-
ble member of the genus that was available for analysis, the
allopatric species M. gelidus, fell outside of the ice worm
clade in 28S rRNA comparisons. Mesenchytraeus gelidus
(“snow worm”) has been recorded on Mt. Rainier, Washing-
ton (Welch 1916a), as well as Yosemite National Park in
California (Aitchison 1977), and can survive in seasonal
snowpack. The widespread distribution of the snow worm
M. gelidus and also M. altus (Welch 1917b) makes the tran-
sition from a snow-dwelling ancestor feasible, in terms of
punctuated evolutionary steps (e.g., Gould and Eldredge
1993) and physical proximity to glacial habitats. On the
other hand, snow worms could have descended from a
glacier-dwelling ancestor. Species of snow worms (i.e.,
M. gelidus,M. altus,M. hydrius, and Moore’s Mesenchy-
traeus niveus) lack intestinal diverticula, suggesting a more
derived relationship to others in this genus, although this
may simply be an expression of a neotanous state. Other de-
scribed members of the genus Mesenchytraeus are morpho-
logically and ecologically very different from ice worms
(e.g., Welch 1919, 1920).
The northern and southern ice worm clades appear to be
reproductively isolated from each other, as imposed by geo-
graphic separation and supported by genetic and morpholog-
ical evidence. The genetic distances between northern and
southern populations are comparable with species-level di-
vergences based on COI comparisons in naidid worms (Bely
and Wray 2004). Moreover, the northern and southern ice
worm clades are nearly as distant to each other as they are to
M. pedatus (Fig. 3), an ecologically and morphologically
very distinct species. At the same time, the two clades ap-
pear to be derived from an ancestor more recent than other
members of the genus examined in this study, arguing
against convergent evolution. Collectively, these observations
suggest that the northern and southern clades are allopatric
subspecies under biological, morphological, and phylogen-
etic concepts produced through geographic isolation (i.e.,
not capable of producing offspring in nature, morphologi-
cally distinguishable, and sharing a unique genetic history).
The time frame of ice worm origins and their putative
split into northern and southern lineages remain unclear, but
these could be estimated once an appropriate molecular
clock is established (perhaps by correlating genetic and geo-
graphic distances between contiguous population pairs
throughout their range). Nonetheless, their relatively long
geographic range coupled with an apparent mode of active
dispersal (~10 m/year for other oligochaetes; Marinissen and
van den Bosch 1992) suggests that ice worms probably
endured the periodic Ice Ages of the Quaternary Period
(~2.4 million years ago to present), and are potentially much
more ancient than that.
We thank David Hibbett, Todd Livdahl, Deborah Robert-
son, Denis Larochelle, and others at Clark University for
their advice and support; Manfred Binder, Zheng Wang, and
Andrew Wilson for their patience and assistance; Kathryn
Coates of the Bermuda Biological Research Station, Tarmo
Timm of the Estonian Agricultural University, Steve Fend of
the USGS Water Resources Division, Stuart Gelder of Uni-
versity of Maine at Presque Isle, and Christer Erséus of the
Swedish Museum of Natural History for sharing their tech-
nical expertise and for help obtaining specimens; and Boggs
Visitors Center (Chugach National Forest), Roberta Holden,
Sheila Byers, and the Vancouver Natural History Society for
ice worms. Funding for P.H.’s 2003 field research was pro-
vided by a research grant from the American Alpine Club.
We also thank Mauri Pelto for his assistance, technical ex-
pertise, and encouragement during the 2002 fieldwork, as
well as the innumerable friends and strangers who provided
rides, good company, food, and drink throughout Montana,
Alberta, British Columbia, and Alaska. We are indebted to
the rangers and management of Denali, Glacier, Glacier Bay,
Mt. Rainier, North Cascades, Olympic, Wrangell – St. Elias,
and Yosemite National parks for permits and advice and the
rangers and management of Chugach, Gifford Pinchot, Inyo,
Mt. Baker – Snoqualmie, Mount Hood, Shasta, Deschutes,
Tongass National Forests for their support and advice. Most
of all, unlimited thanks and respect go to our families for
their support and patience, especially Charity Scott who has
put up with more than her share.
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Hartzell et al. 1213
... Perhaps no species is more directly tied to ice sheets than glacier ice worms, Mesenchytraeus solifugus in North America [18] and Sinenchytraeus glacialis in Tibet [19]. The geographical range of M. solifugus (hereafter 'ice worm') follows a coastal arc from the Chugach Mountains in southeast Alaska to the Cascade Volcanoes of Washington and Oregon [20]. Ice worms cannot tolerate temperatures more than roughly +78C from freezing and require glacier ice for survival and reproduction [21]. ...
... Previous genetic studies based on one or two genetic markers identified three ice worm lineages: a 'northern' clade in southern Alaska, a 'central' clade in southeast Alaska and northern British Columbia, and a 'southern' clade ranging over much of British Columbia to southern Oregon [20,21,23]. Surprisingly, phylogenetic evidence supported the northern and southern lineages as being most closely related to one another despite the central clade separating them geographically. ...
... We described two genetic groupings (I and II) which are described with respect to the crest of the Coast Mountains, where ice ridges formed during the Pleistocene [25]. While the phylogenetic data used in this study (i.e. the lack of an outgroup) preclude us from diagnosing groups I and II as monophyletic, given the results of previous studies [20,21,23], we predict that future efforts will diagnose them as such, perhaps even representing two nascent species. Finally, our genomic data lend support to the glaciological record in the region, adding a biological line of evidence to a postulated key north-south dividing line along the crest of the Coast Mountains where ice ridges likely formed during the Pleistocene and repeatedly propagated ice flow to the east and west [25]. ...
Disentangling the contemporary and historical factors underlying the spatial distributions of species is a central goal of biogeography. For species with broad distributions but little capacity to actively disperse, disconnected geographical distributions highlight the potential influence of passive, long-distance dispersal (LDD) on their evolutionary histories. However, dispersal alone cannot completely account for the biogeography of any species, and other factors-e.g. habitat suitability, life history-must also be considered. North American ice worms ( Mesenchytraeus solifugus) are ice-obligate annelids that inhabit coastal glaciers from Oregon to Alaska. Previous studies identified a complex biogeographic history for ice worms, with evidence for genetic isolation, unexpectedly close relationships among geographically disjunct lineages, and contemporary migration across large (e.g. greater than 1500 km) areas of unsuitable habitat. In this study, we analysed genome-scale sequence data for individuals from most of the known ice worm range. We found clear support for divergence between populations along the Pacific Coast and the inland flanks of the Coast Mountains (mean FST = 0.60), likely precipitated by episodic ice sheet expansion and contraction during the Pleistocene. We also found support for LDD of ice worms from Alaska to Vancouver Island, perhaps mediated by migrating birds. Our results highlight the power of genomic data for disentangling complex biogeographic patterns, including the presence of LDD.
... Enchytraeidae are small oligochaete worms (6-50 mm in length), adapted to semiterrestrial and terrestrial environments ( Christensen & Glenner 2010 ), including intertidal sands and ice sheets Hartzell et al . 2005 ). They show a global distribution from the Arctic to the tropics ( Nurminen 1965 ;Petersen & Luxton 1982 ;Standen 1988 ;Didden 1993 ). Up to 700 species have been described, of which 650 are considered valid ( Erséus 2005 ). Traditionally, they are assumed to be mainly microbivores ( Didden 1993 ). Recent research sustains that they are ...
... raits have also played an important role in shaping enchytraeid communities. For example, the more diverse enchytraeid communities in the Arctic tundras are characterized by a high degree of endemism which indicates an undisturbed long history ( Christensen & Dózsa-Farkas 2006 ). This has led to the suggestion that enchytraeids are slow dispersers ( Hartzell et al . 2005 ) and that the most likely sources of postglacial colonization were glacial refugia ( Christensen & Dózsa-Farkas 2006 ). ...
... Es bastante lo que se ha escrito y se conoce sobre la biodiversidad en el entorno de los glaciares, pero es más bien escaso lo que se sabe de la presencia de especies en los glaciares mismos, vale decir, de formas de vida que realizan todo su ciclo vital en los glaciares (ver Figuras 3 y 4). Se ha comprobado que existe vida en glaciares (ver, por ejemplo, Hartzell et al., 2005;Takeuchi, 2001) por organismos adaptados a este ambiente extremo. Y si bien ello es una capacidad que importa a la humanidad, como moderada durante toda la estación estival, y contribuyen con agua a sus cuencas. ...
... Pero solamente así se podrá extraer agua de los glaciares cuando se necesite (Figura 6), y reponer esas extracciones en años de mayor abundancia de las precipitaciones para, de esa manera, conservar los glaciares para el futuro y para que continúen sirviendo a los ecosistemas de montaña. por ejemplo el empleo por los gusanos de hielo de proteínas anticongelantes que resisten el frío (Hartzell et al., 2005), es poco lo que se ha avanzado en el conocimiento de la biodiversidad en los glaciares mismos y en cómo esta biodiversidad afecta el balance de masa de los glaciares (Takeuchi et al., 2002). ...
Los glaciares importan en los ecosistemas de montaña por diversas razones, pero algunas de las más relevantes se refieren a los riesgos que la presencia de ellos origina, al aporte hídrico que ellos realizan, y por su contribución al mantenimiento de los ecosistemas. Actualmente, existen metodologías y modelos, y la tecnología necesaria, como para estimar correctamente la mayoría de los riesgos generados por glaciares. Sin embargo, persiste un aspecto importante aún muy incierto. Se refiere a la presencia y extensión de la morrena de fondo en los glaciares y al control esencial que ella ejerce sobre la estabilidad mecánica de las masas de hielo. Los glaciares se consideran a menudo como reservas de agua, aun cuando existe consenso en que el futuro de ellos es la extinción. Los glaciares aportan agua a sus cuencas en la medida que pierden masa de hielo, que es lo que produce su paulatina reducción. Si queremos que los glaciares persistan, debemos hacer algo para modificar sus balances de masa negativos hasta hacerlos al menos neutro; pero esto implica, necesariamente, un cero aporte de agua desde los glaciares a sus cuencas. De allí un dilema que debemos resolver: ¿queremos que continúe el aporte hídrico de los glaciares hasta su desaparición, o estamos dispuestos a hacer algo para que sobrevivan aceptando que, desde ya, dejarán de contribuir agua? Junto a esta inquietud, es importante avanzar en el manejo de los glaciares. En cuanto a la biodiversidad, se ha comprobado que existe vida en glaciares por organismos adaptados a este ambiente extremo. Y si bien ello es una capacidad que importa a la humanidad, es poco lo que se ha avanzado en el conocimiento de la biodiversidad en los glaciares mismos. Finalmente, la protección de glaciares es algo sobre lo cual parece no existir dudas en la mayoría de las sociedades del mundo, sin embargo ha sido difícil acordar una definición de glaciares y sus entornos, vale decir, de lo que queremos proteger.
... Such compost would be continuously discharged, along with sediments that lead to the formation of terminal moraines, as glaciers continue to plough the land in their seasonal advance and retreat. 9 The idea of the cryosphere as compost is not entirely removed from reality, knowing how in many regions of the world, such as the Arctic, glacial ice holds worms that crawl up at night to feed from algae growing in snow, which, in turn, become prey to passing birds, very much as occurs in soil (Hartzell et al., 2005;Benn and Evans, 2010;Taillant, 2015). Far from being homogeneous and inert, ice resembles soil's heterogeneity and animation. ...
A tension between solidity and fluidity tends to divide the sciences and the humanities along lines that define what is hard and soft in knowledge. This divide relates to similar dichotomies, between exteriority and interiority, material and spiritual, homogeneity and heterogeneity, matter and form, all of which have been partially mapped in Western thinking onto a traditional separation between earth and sky. Yet particular forms of knowledge sit uneasily within these tensions, a paradigmatic example of which is an understanding of solids as ‘viscous fluids’. This article explores the concept of viscosity, attending to how it has impacted on understandings of matter, as well as broader social and cultural issues. It does so, particularly, by looking into the scientific study of ice, a material that has historically been regarded as solidfluid, to argue that life and sociality remain possible only in so far as matter that is viscid allows solid and fluid states to mingle.
... Ice worms consume algae (Goodman, 1971;Murakami et al., 2015) but it is currently unknown if their grazing substantially impacts algal abundance. Future studies should compare algae abundance on glaciers with and without ice worms (e.g., in southeast Alaska; Dial et al., 2012;Hartzell et al., 2005) to investigate this relationship. Another dark-bodied invertebrate-springtails (subclass Collembola)-are much smaller than ice worms but can be present at densities >5,000 m 2 during daylight (Mann et al., 1980). ...
The global cryosphere, Earth's frozen water, is in precipitous decline. The ongoing and predicted impacts of cryosphere loss are diverse, ranging from disappearance of entire biomes to crises of water availability. Covering approximately one-fifth of the planet, mass loss from the terrestrial cryosphere is driven primarily by a warming atmosphere but reductions in albedo (the proportion of reflected light) also contribute by increasing absorption of solar radiation. In addition to dust and other abiotic impurities, biological communities substantially reduce albedo worldwide. In this review, we provide a global synthesis of biological albedo reduction (BAR) in terrestrial snow and ice ecosystems. We first focus on known drivers—algal blooms and cryoconite (granular sediment on the ice that includes both mineral and biological material)—as they account for much of the biological albedo variability in snow and ice habitats. We then consider an array of potential drivers of BAR whose impacts may be overlooked, such as arthropod deposition, resident organisms (e.g., dark-bodied glacier ice worms), and larger vertebrates, including humans, that transiently visit the cryosphere. We consider both primary (e.g., BAR due to the presence of pigmented algal cells) and indirect (e.g., nutrient addition from arthropod deposition) effects, as well as interactions among biological groups (e.g., birds feeding on ice worms). Collectively, we highlight that in many cases, overlooked drivers and interactions among factors have considerable potential to alter BAR, perhaps rivaling the direct effects of algal blooms and cryoconite. We conclude by highlighting knowledge gaps for the field with an emphasis on the underrepresentation of genomic tools, understudied areas (particularly high-elevation glaciers at tropical latitudes), and a dearth of temporal sampling in current efforts. We detail a global framework for long-term BAR monitoring that, if implemented, would yield a tremendous amount of insight for BAR and would be particularly valuable in light of the rapid ecological and physical changes occurring in the contemporary cryosphere.
... Studies (reviewed by Kaczmarek et al., 2016) of cryoconite holes report ammonia-oxidizing archaea, nitrogen-fixing bacteria, filamentous cyanobacteria (Oscillatoriaceae) which bind with mineral particles, ciliated protozoa, diatoms (Stanish et al., 2013), purple, red, and orange-colored green algae, as well as a variety of snow and ice fungi. Obligate-glacier dwelling animals include cryoconite copepods (Hexanauplia: Copepoda: Glaciella yalensis Kohshima, 1987;Kikuchi, 1994;Takeuchi et al., 2000) and flightless midges (Insecta: Diptera: Chironimidae: Diamesinae; Kohshima, 1984) on Himalayan glaciers; semi-flightless midges (Insecta: Diptera: Chironimidae: Podomoninae) on New Zealand glaciers (Odell, 1956;Dumbleton, 1973;Boothroyd and Cranston, 1999); two species of stoneflies (Insecta: Plecoptera: Gripopterygidae) in Patagonia (Kohshima, 1985;Vera et al., 2012;Murakami et al., 2018;Pessacq and Rivera-Pomar, 2019); springtails (Insecta: Collembola; Fjellberg, 2010) worldwide; glacier ice worms (Annelida: Oligochaeta: Enchytraeidae) in North America's Pacific northwest (Wright, 1887;Emery, 1898;Tynen, 1970;Goodman, 1971;Shain et al., 2001;Hartzell et al., 2005;Dial et al., 2012;Dial et al., 2016) and Tibet (Liang, 1979); nematodes in Antarctica (Mueller et al., 2001) and Europe (Azzoni et al., 2015); as well as nearly pan-glacial (Zawierucha et al., 2015) tardigrades (Desmet and Vadrompus, 1994;Zawierucha et al., 2016) and rotifers (Desmet and Vadrompus, 1994;Porazinska et al., 2004;Kaczmarek et al., 2014). Facultative-glacier dwelling organisms include moss and the animals associated with that habitat such as rotifers, tardigrades, mites, and collembola . ...
If nutrients and a carbon source are available, life as we know it can actively reside nearly anywhere liquid water exists-even glacier ice and snow (Zawierucha et al., 2015). Just as with tropical rainforests, temperate grasslands, and polar tundra, the worldwide collection of glacial ecosystems residing on permanent freshwater ice can be considered as a biological biome (Anesio and Laybourn-Parry, 2012). In fact, all kingdoms of life (Ruggiero et al., 2015) have been found living on glacier surfaces, a land cover that extends over 1.6 × 107 km2 (Williams Jr. and Ferrigno, 2012), or 10% of the Earth's surface. The presence of these organisms living on glaciers leads to melting, and the melt-water they create is necessary for their existence, making the glacier biome important from a global warming perspective (Ganey et al., 2017). While all of the world's glaciers have much microbial life in common, especially single-celled algae, the taxonomic orders of glacier-dwelling macro-invertebrates differ across continents.
... Our contextual isotope data indicate multiple trophic level interactions in supraglacial ecosystems. Ice worms (Mesenchytraeus solifugus) are a species of oligochaetes adapted to live solely in snow and ice with a range of low-elevation, temperate glaciers from south-central Alaska to central Oregon (Hartzell et al., 2005;Dial et al., 2016). Ice worms tolerate a narrow range of temperatures (À6.8 to 5°C; Edwards, 1985), and it has been suggested that ice worms feed primarily on snow algae, coming out at night to feed and then retreating into the glacier for protection from high temperatures during the day (Goodman, 1971). ...
Full-text available
Earth has experienced periodic local to global glaciation for nearly 3 billion years, providing supra- and subglacial environments for colonization by microbial communities. A number of studies have reported on the role of microbial communities in glacial ecosystems including their influence on element cycling and weathering, but there is a paucity data on volcanic rock-hosted glacial ecosystems. Glaciers on stratovolcanoes in the Pacific Northwest override silica-rich rocks which represent analogues to an early Martian cryosphere. On these glaciers, blooms of photosynthetic snow algae support supraglacial microbial communities as has been observed on snowfields, glaciers, and ice sheets. In subglacial environments of volcanic rock-hosted glacial systems, weathering is driven, at least in part, by carbonic acid, suggesting a link between supraglacial carbon sources and subglacial heterotrophic microbial communities. Here, we report inorganic carbon assimilation and microbial community composition on glaciers across three stratovolcanoes ranging in composition from dacitic to mafic in the Pacific Northwest of the United States to begin to constrain the role of supraglacial primary productivity in subglacial weather processes. These data, coupled to contextual carbon and nitrogen isotope analyses of biomass and aqueous geochemistry, indicate snow algae drive light dependent carbon uptake across supraglacial and periglacial environments. Furthermore, snow algae microbial communities are supported by fixed nitrogen predominantly from deposition via precipitation. Our data highlight intense cycling of carbon and nitrogen driven by supraglacial microbial communities that feeds subglacial microbial communities which in turn may drive weathering processes. These results further underscore the role of glacial ecosystems in global biogeochemical cycling, especially during past global glaciations. Finally, these results lend support for glaciers as refugia for biodiversity on Earth and potentially on other bodies such as Mars where evidence exists for widespread and long-lived cryosphere including glaciers and ice sheets.
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Marionina Michaelsen, 1889, is distributed worldwide and inhabits marine, terrestrial, and limnic environments. Marionina coatesae Erséus, 1990 of the present study is characterized by two characteristics: two chaetae per segment all over the body except in segment XII and round or oval­shaped spermathecal ampullae with sperm rings irregularly scattered on the walls. Korean specimens of the species were obtained from the intertidal sand beach of the East Sea in Korea. Here, M. coatesae is reported for the first time in Korean fauna as the first marine oligochaete, microdriles, species.
Full-text available
Disentangling the contemporary and historical factors underlying the spatial distributions of species is a central goal of biogeography. For species with broad distributions but little capacity to actively disperse, disconnected geographic distributions highlight the potential influence of passive, long-distance dispersal (LDD) on their evolutionary histories. However, dispersal alone cannot completely account for the biogeography of any species, and other factors - e.g., habitat suitability, life history - must also be considered. North American ice worms ( Mesenchytraeus solifugus ) are glacier-obligate annelids that inhabit coastal North American glaciers from Oregon to Alaska. Previous studies identified a complex biogeographic history for ice worms, with evidence for genetic isolation, unexpectedly close relationships among geographically disjunct lineages, and evidence for contemporary migration across large (>1,500 km) areas of unsuitable habitat. In this study, we collected genome-scale sequence data for most of the known ice worm range. We found support for a deep divergence between populations along the Pacific Coast and the inland flanks of the Coast Mountains (mean F ST = 0.60) as well as support for LDD from Alaska to Vancouver Island, perhaps mediated by migrating birds. Our results highlight the power of genomic data for disentangling complex biogeographic patterns, including the presence of LDD.
Full-text available
We examined the impact of three forms of dispersal, stepping-stone, normal and leptokurtic, on spatial genetic structure of expanding populations using computer simulations. When dispersal beyond neighbouring demes is allowed, rare long-distance migration leads to the establishment of pocket populations in advance of the main invasion front and results in spatial clustering of genotypes which persists for hundreds of generations. Patchiness is more pronounced when dispersal is leptokurtic as is the case in many animal and plant species. These results are of particular interest because population genetic parameters such as gent flow and effective population size are commonly estimated using gent frequency divergence information assuming equilibrium conditions and island models. We show how the three forms of dispersal during colonization bring about contrasting population genetic structures and how this affects estimates of gene flow. The implications for experimental studies of the spatial dimension of population genetic structure are discussed.
During the Fraser (Late Wisconsin) Glaciation, the Cordilleran ice sheet advanced southward from source areas in British Columbia and terminated in the United States between the Pacific Ocean and the Continental Divide. The ice sheet extended farthest along major south-trending valleys and lowlands that traverse the international boundary; it formed several composite lobes segregated by highlands and mountain ranges. Each lobe dammed sizable lakes that drained generally southward or westward along ice margins and across divides. Field evidence warrants considerable revision of the ice margin in northern Idaho and northeastern Washington. -from Authors
The ice worm, Mesenchytraeus solifugus ssp. rainierensis, is the only known annelid that survives in glacier ice. We report the locations of eight ice worm populations in south-central Alaska, including the northern- and western-most extent of known ice worm habitation. All ice worms identified in this study inhabit coastal glaciers proximal to the Gulf of Alaska. They were found in a variety of habitats including level snowfields, steep avalanche cones, crevasse walls, glacial rivers and pools, and hard glacier ice. Ice worms were not found on all coastal glaciers nor were they found in Alaska's interior (the Alaska Range). Ice worms on Byron Glacier, Alaska, totaled similar to 30 million and were distributed on seven distinct avalanche cones. They displayed a diurnal cycle, appearing on the glacier surface several hours before sunset and penetrating back into the glacier shortly after sunrise. Experiments suggest that ice worms preferentially penetrate the glacier beneath surface algae, Chlamydomonas nivalis, to a depth between 15 and 100 cm and resurface at a proximal location. Lateral movement of ice worms on the glacier surface can reach speeds of similar to3 m/h. Ice worms on Byron Glacier avoided light, but did not respond preferentially to different wavelengths in the visible spectrum. Finally, ice worms displayed an unexpected attraction to heat.