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BIOLOGIJA. 2012. Vol. 58. No. 4. P. 245–255
© Lietuvos mokslų akademija, 2012
Tardigrades (Tardigrada) in Baltic States
Ingrida ŠATKAUSKIENĖ
Department of Biology,
Vytautas Magnus University,
Vileikos 8, LT-44404 Kaunas,
Lithuania
* Corresponding author. E-mail: i.satkauskiene@gmf.vdu.lt
e tardigrades (Tardigrada), one of the micrometazoans groups,
are reviewed. Tardigrades are distributed almost everywhere: in
moss, lichens, soil, in niches of freshwater and seawater. e abi-
lity of tardigrades to undergo cryptobiosis has aroused interest
among world scientists who would like to apply this mechanism
to other biological systems that might benet from dry storage
in extreme conditions. is paper reviews the latest information
on tardigrades taxonomy and phylogenetic position, distribution,
some aspects of their biology, reproduction and life history. e
present work also provides the data of research of tardigrades in
the Baltic states.
Key words: tardigrada, eutardigrada, heterotardigrada, freshwa-
ter, life history, anhydrobiosis, cryptobiosis
INTRODUCTION
Scientic knowledge of invertebrates varies from
group to group. e best-studied groups are in-
sects, crustaceans and mollusks. Even in these
well-studied groups, there are huge information
gaps, especially for smaller animals and those liv-
ing in developing countries or underground habi-
tats (Strayer, 2006). Little is known about “minor”
phyla: bryozoans (Ryland, 2005; Dunn et al., 2008;
Massard, Geimer, 2008), gastrotrichs (Balsamo et
al., 2008; Kieneke et al., 2012; Paps, Riutort, 2012),
nematomorphs (Hanelt et al., 2005; Poinar, 2008)
and freshwater tardigrades (McFatter et al., 2007;
Garey et al., 2008; Meyer, 2011). Meanwhile some
of these groups are widespread and abundant.
For example, gastrotrichs probably occur in most
freshwater habitats throughout the world (Strayer,
2006). e tardigrades are one of most abundant
invertebrates in moss and lichens, meanwhile lit-
tle is known about the tardigrades in the Baltic
countries.
Some of these micrometazoans could be used
as bioindicators, as model organisms for studies of
development mechanisms or for experiments in
the open space.
Tardigrades are referred to as one of the “lesser-
known” groups of micrometazoans (Nelson, 2002;
Romano, 2003). Presently, the exact number of
various Tardigrada species is unknown. In order
to increase knowledge about these invertebrates
and also to explore the possible biotechnological
246 Ingrida Šatkauskienė
and biomedical applications of their bio logy,
more economic and human resources need to
be focused on this group (Guil, Cabrero-Sañudo,
2007). e aim of this study was to summarize the
latest information on tardigrades biology, signi-
cance and provide the most recent research data
on tardigrades in the Baltic States.
Some aspects of tardigrade biology
Tardigrada is known as “water bear” that bears
this descriptive name based on the animal’s lum-
bering gait (tardi – slow, grade – walker) and also
because these invertebrates usually live in water.
Tardigrades are one of the smallest metazoa and
their size is close to that of rotifera, gastrotricha
or microscopic nematodes. Body length of adult
tardigrade is approximately 250–500 µm (Nel-
son, 2002). Like in the arthropods, the body of
tardigrades is covered by cuticle. External layer
of cu ticle is so, lacks calcium and is built from
a protein albuminoid which diers from chitin
(Gagyi-Paly, Stoian, 2011). e inner layer of
the cuticle contains chitin. Tardigrades molt and
change their cuticle like the arthropods. Molting
occurs every ve to ten days throughout the tardi-
grade’s life (Nelson, 2002).
Water bear may be detritovorious, bacterio-
vorous, carnivorous and herbivorous (Romano,
2003). Irrespective of the wide range of food con-
sumption, tardigrades do not display a great va-
riation in the organization of the digestive system.
e tardigrade buccal–pharyngeal apparatus that
is used to suck out the content of cells is a complex
structure with a considerable taxonomic signi-
cance among taxa belonging to several taxonomic
levels, particularly in the eutardigrades (Pilato,
Binda, 2010). e buccal–pharyngeal apparatus
consists of cuticular structures such as a buccal
ring, a buccal tube with apophyses for muscle at-
tachments, stylets and a muscular sucking phary-
nx (containing placoids) (Nelson et al., 2010; Gui-
detti et al., 2012) (Fig. 1).
During the last decade various aspects of
anatomy and physiology of Tardigrada have been
studied. Greven (2007) provided information on
the visual organs of tardigrada. Many Eutardi-
grada and some of Echiniscidae possess inverse
pigment-cup ocelli, which are located in the outer
lobe of the brain, and probably are of cerebral ori-
gin (Fig. 2). Depending on the species, response
to light (photokinesis) is negative, positive or in-
dierent and may change during the ontogeny.
Greven (2007) states that the homology of the
tardigrade eyes with the visual organs of other bi-
laterians is dicult to establish and further com-
parative studies are needed.
Fig. 1. General structure of buccal apparatus of eutar-
digrade. m, mouth; bt, buccal tube; s, stylets (which
serve as a tool to pierce plant cells); ss, stylet supports;
ph, pharynx; pl, placoids
Fig. 2. e anterior part of the body of tardigrade with
two eyes (arrows)
247
Tardigrades (Tardigrada) in Baltic States
e analysis of the nervous system of Tar-
digrada plays an important role considering
the phylogenetic anities of the groups (Dewel,
Dewel, 1996, 1997; Nielsen, 2001). Although the
central nervous system of tardigrades is general-
ly described as belonging to the rope-ladder-like
type comprised of ganglia with connectives and
commissures, unambiguous documentation of
commissures is almost absent in the literature
(Zantke et al., 2008). Meanwhile the use of more
neuroanatomical data of Tardigrada should con-
tribute to our understanding of tardigrade phylo-
genetic anities in a more global approach con-
sidering a variety of morphological and molecular
data (Zantke et al., 2008).
Considering the reproduction system of tar-
digrades it is noteworthy that it is variable and
species-dependent, it may be dicoeciuos, her-
maphroditic and may reproduce in sexual or par-
thenogenetical way. Using cryptobiosis and passive
dispersal, parthenogenesis is favorable in coloniz-
ing new, isolated and unstable habitats, as begin-
ning with a single individual is all that is required
(Altiero et al., 2006). For marine species (mainly
heterotardigrades) parthenogenesis is unknown,
meanwhile in limno-terrestrial tardigrades always
appear continuous (Bertolani, 2001). Herma-
phro ditism in limno-terrestrial species occurs in
several eutardigrade families (Pilato et al., 2006)
and in Heterotardigrada only one species is her-
maphroditic (Bertolani, 2001). Hermaphroditism
is not common in tardigrades, indicating that this
model of reproduction is a less frequent sexual
condition. e ndings of a hermaphroditic spe-
cies conrm that in tardigrades this condition
develops independently in dierent evolutionary
lines (Pilato et al., 2006).
Sexual dimorphism was established for one
species of Heterotardigrada – Echiniscus mauccii
(Mitchell, Romano, 2007) and three other Echinis-
cus species (Miller et al., 1999). Females, distin-
guished by their gonopore, are larger than males
(Mitchel, Romano, 2007). Similar sexual dimor-
phism (females are larger than males) is observed
in two eutardigrada species: Macrobiotus richtersi
and Hypsibius convergens (Guidetti et al., 2007).
Data covering the gametogenesis of Tardigrada is
especially scarce (Poprawa, 2005).
Reproduction of tardigrades is coupled with
molt. e female subsequently moults, laying her
eggs in the shed cuticle (Fig. 3). Gonad size is con-
strained by the cuticle capacity and by the gut size
(food source) that competes for the space within
the body cavity (Guidetti et al., 2007).
All tardigrada produce eggs, which consist of
polysaccharides, peptides and lipids (Poprawa,
2005) and are oen essential for a correct iden-
tication of tardigrada species (Fig. 4a, 4b, 4c)
(Cromer et al., 2007).
e behavior and chemical communication at
the time of reproduction of tardigrades are un-
known. e information on the origin and rele-
Fig. 3. Many tardigrades store their eggs underneath
the cuticle, aerwards shed them along with the cuticle
when moulting
Fig. 4a. e egg of Richtersius coronifer found in moss
Bryum sp.
248 Ingrida Šatkauskienė
vance of sex steroid receptors in invertebrates are
still limited (Köhler et al., 2007).
Parental care is not common in tardigrades,
however Pilato et al. (2006) mentioned that new-
borns of Hypsibius zetlandicus (Eutardigrada) are
still within the old cuticle of the parent and this
could be an indication of the possibility of “pa-
rental care”.
Time of reproduction is not clear for many
species of tardigrades. Mitchel and Romano
(2007) observed that sexual reproduction of
Echiniscus mauccii continues for the entire year
and suggested that this species has classic K-se-
lected traits.
Life history traits are always very interesting
subjects in the study of animal adaptation and
evolution. Despite this importance, literature data
on the life history traits and population dynamics
of freshwater and semiterrestrial species of tardi-
grades are scanty and fragmentary (Mitchell, Ro-
mano, 2007), while actually no data are available
for marine species (Altiero et al., 2006).
Distribution and habitats of tardigrades
e phylum Tardigrada has a worldwide distribu-
tion (Nelson, 2002; Bertolani et al., 2004) that is
related with the ability of Tardigrada to survive
in extreme environments and to use cryptobio-
sis together with passive dispersal and partheno-
genesis. eoretically, parthenogenesis allows the
colonization of new and remote territories begin-
ning with a single individual (Miller, Heatwole,
1996; Bertolani, 2001). Despite this possibility to
spread, a very high number of tardigrada species
have limited geographical distribution and are
adapted to restricted microenvironmental condi-
tions (Pilato et al., 2006).
Tardigrades use various habitats: marine and
estuarine, freshwater and terrestrial. Informa-
tion on the distribution and ecology of limno-
terrestrial Tardigrada is scarce (McFatter et al.,
2007). ey are benthic or crawl on water vege-
tation. Most species live in the littoral zone (Nel-
son, 2002). e majority of these organisms are
not real hidrophylous and are found in terrestrial
and aquatic environments. Numerically, limno-
terrestrial tardigrades comprise a minor com-
ponent of benthic invertebrate communities.
Knowledge is lacking about their tropic relation-
ships or dispersal in benthic habitats (McFat-
ter et al., 2007).
Terrestrial tardigrades are inhabitants of mo-
sses, lichens, soil and leaf litter. Tardigrades in
leaf litter from beech forests (Guidetti et al., 1999)
and soil (Bertolani et al., 1996; Nelson, 2002) ex-
hibit high species diversity and high densities, but
the evidence of tardigrades for substrate speci-
city is weak. Many species of tardigrades may be
present in soil and leaf litter, but few were found
only in these substrates (Meyer et al., 2007). Jöns-
son (2003) indicated that dierent mosses’ growth
Fig. 4c. e egg of Macrobiotus hufelandi found in
moss Bryum sp.
Fig. 4b. e egg of Macrobiotus richtersii (?) found in
moss Pleurozium schreberi
249
Tardigrades (Tardigrada) in Baltic States
form might have an impact on tardigrada abun-
dance. Meyer (2006; 2007) noted that some tar-
digrada species were signicantly associated with
mosses or foliose lichens in general, but no sig-
nicant association was detected between a tardi-
grada species and a substrate species.
Tardigrada densities in soil are high and may
vary from 300 to 33,600 individuals in m2 (Hoh-
berg, 2006). Soil-inhabiting tardigrades have high
metabolic rates, hence they are sensitive to subtle
environmental variances and respond to structu-
ral changes in the soil (Harada, Ito, 2006).
ere are few studies on the relation of tardi-
grada diversity and richness and season. Some
scientists have proposed that tardigrada commu-
nities are stable through time and there are not
signicant dierences comparing the tardigrada
density and community structure between dif-
ferent seasons (Peluo et al., 2006). Meanwhile
McFatter (2007) mentioned that the density of
Nearctic freshwater tardigrada species peaks up
in the spring and / or fall. is disagreement indi-
cates that more studies and more data are needed
in this eld.
Taxonomy and phylogeny
More than one thousand of Tardigrada species
were included in the recently published checklist
(Degma et al., 2009–2012). Based on morpho-
logical characteristics, the phylum of tardigrada is
divided into two major classes: Heterotardigrada
(armored tardigrades) and Eutardigrada (naked
tardigrades) (Nichols et al., 2006).
e exact number of species of tardigrades is
not known because of insucient eorts invested
in the tardigrades compared to other invertebrates
(such as Insecta: Coleoptera), and that there is
a need of engagement of more taxonomists and
more extensive sampling areas (Guil, Cabrero-
Sañudo, 2007).
Dormancy of tardigrades: anhydrobiosis
Dormancy is an important adaptation strategy
that allows many organisms to survive in unfavo-
rable environmental conditions. Tardigrades have
two forms of dormancy, namely cryptobiosis and
encystment.
Tardigrades and some others organisms (Ne-
matoda, Rotifera) are capable of entering a latent
state (cryptobiosis) when environmental condi-
tions are unfavorable, e. g. freezing, desiccation,
low oxygen tension, and salinity variations. When
tardigrada are in a latent state, their metabolism
is reduced. In contrast to death, cryptobiosis is a
reversible state and as soon as environmental con-
ditions change, tardigrada return to life (Neuman,
2006). Five types of cryptobiosis are distinguished:
encystment, anoxybiosis, cryobiosis, osmobiosis
and anhydrobiosis (Nelson 2002; Bertolani et al.,
2004; Watanabe, 2006).
To remain active, all tardigrades require water.
One type of cryptobiosis, namely anhydrobiosis,
is induced by water loss and occurs in eggs, ju-
veniles and adults of terrestrial eutardigrades and
echiniscids (Nelson, 2002; Rebecchi et al., 2007).
Anhydrobiotic tardigrades always shrink in struc-
ture resembling “tun” when dehydrated (Wright,
2001; Bertolani et al., 2004; Watanabe, 2006).
When tardigrades are desiccated at a low relative
humidity or under anoxia they cannot form tun
and be revived (Watanabe, 2006). Various species
of tardigrada are characterized by interspecic
dierences in cryptobiotic (anhydrobiosis and
cryobiosis) survival possibility (Jönsson et al.,
2001; Bertolani et al., 2004).
Jönsson and Rebecchi (2002) indicate that the
phenotypic state of the individuals has an impact
on the probability to survive a period of anhydro-
biosis. Eects of body size on anhydrobiotic sur-
vival suggest age – specic selection, and eects
of energy status indicate that energy allocations to
anhydrobiotic functions are also object to selec-
tion of evolution (Bertolani et al., 2004).
Biochemical mechanism of cryptobiosis (an-
hydrobiosis) is also an object of interest. Treha-
lose is known as a common compatible solute in
anhydrobiotic organisms from unicellular orga-
nisms to invertebrates and higher plants. Treha-
lose may provide eective protection against de-
siccation because of its superior biochemical and
phy sicochemical properties for stabilizing mem-
branes and biomolecules including proteins and
lipids (more about anhydrobiosis see review by
Watanabe, 2006).
Trehalose is produced prior to the stages of
anhydrobiosis and cryobiosis. Recently, it has be-
come clear that the phenomenon of cryptobiosis
is much more complex than initially thought to
be. New results show that it is not only trehalose
that is responsible for survival during cryobiosis
250 Ingrida Šatkauskienė
and anhydrobiosis. Some species of tardigrades
produce trehalose in small amounts (2–3% of dry
weight) compared to other invertebrates capable
to devolve anhydrobiotic state (Jönsson, 2007).
Hengherr et al. (2008) revealed signicant dif-
ferences between eight tardigrada species (He-
terotardigrada and Eutardigrada) on the trehalose
levels in dierent states of hydratation and dehyd-
ratation. Trehalose accumulation was found in
some species of Eutardigrada but not detected in
the species Milnesium tardigradum and no change
in trehalose level had been observed in any spe-
cies of Heterotardigrada (Hengherr et al., 2008).
e study of Jönsson and Schill (2007) suggests
that the desiccation cycles of some species of tar-
digrades are related with stress proteins of the
family Hsp70. ese proteins participate in un-
folding and recolonization of proteins damaged
by stresses and protect newly synthesized proteins
from denaturation and aggregation (Watanabe,
2006). is group of proteins may play a role in
the post-anhydrobiotic repair process (Jönsson,
2007). e phenomenon of cryptobiosis, when a
tardigrada can go into a reversible death (ameta-
bolic stage) for many years, and aer a few min-
utes of rehydration can climb around again, might
propose some hints to explain how life developed
on earth.
Signicance of tardigrades
Tardigrades share many characteristics with
Caenorhabditis elegans and Drosophila that could
make them useful as laboratory models, but there
have been few studies of long-term culturing of
tardigrades (Suzuki, 2003). Gabriel et al. (2007)
demonstrated that the tardigrade Hypsibius du-
jardini can be cultured continuously for decades
and can be cryopreserved. It has been reported
that H. dujardini has a compact genome, a little
smaller than that of C. elegans or Drosophila and
can serve as a model for studying the evolution of
developmental mechanisms (Gabriel et al., 2007).
Other signicant feature of tardigrades is their
tolerance to very high doses of ionizing radiation.
Hydrated tardigrades have shown similar or higher
tolerance to irradiation compared to dehydrated,
anhydrobiotic tardigrades (Jönsson, 2007). is
suggests that radiation tolerance in these animals
is not restricted to biochemical protection mecha-
nisms of the dry cells (Jönsson, 2007).
Tardigrades are relatively more vulnerable to
UV irradiation than to γ-irradiation in the hyd-
rated state (Jönsson, 2007). e observed tole-
rance to ionizing radiation, particularly in active
tardigrades, may rely on an ecient DNA repair
system. However, this mechanism of DNA repair
will remain speculative and still must be veried
(Jönsson, 2007).
Tardigrades with abilities to stand complete
desiccation, cold and high levels of ionizing and
UV radiation provide opportunity for studies on
the response of living multicellular organisms ex-
posed to open space (Jönsson, 2007).
Moreover, tardigrades may even be of econom-
ic interest due to their ability to undergo crypto-
biosis, an environmentally resistant state, when
conditions are unfavorable; the substances in-
volved in cryptobiosis have potential applications
in biomedicine and biotechnology (Guil, Cabrero-
Sañudo, 2007). e pharmaceutical industry has
been very interested in the role of sugar trehalose
that tardigrades produce prior to the stages of
anhydrobiosis and cryobiosis. Trehalose appears
to protect the cellular membranes of tardigrades
against the damage of freezing and dehydration
and therefore provide stability for biological pro-
ducts (Crowe et al., 1996). Vaccines and restriction
enzymes can be stored in a trehalose formulated
dry state at +70 °C for one month without lost ac-
tivity (Colaco et al., 1992). A number of biological
products (monoclonal antibodies; pharmaceuti-
cal, foodstu) have been stabilized using trehalose
(Guo et al., 2000). Trehalose may be used in or-
gan transplantation to avoid freezing damage and
to safely preserve human eggs and those of en-
dangered species, giving better options to young
women facing cancer therapies that may leave
them infertile and others who simply want to delay
reproduction. Introduction of sugars into cells and
into oocytes can protect them against freezing-as-
sociated stresses. Researchers injected the eggs of
mouse with trehalose, cooled them to liquid nitro-
gen temperature, thawed them and exposed them
to sperm. ey got healthy babies at a similar rate
to unfrozen controls (Eroglu et al., 2003).
ese microscopic metazoans are signicant
as bioindicators of environmental pollution. Most
terrestrial tardigrades live in mosses and lichens.
Numerous studies proved that mosses are valuable
bioaccumulators and the concentrations of the
251
Tardigrades (Tardigrada) in Baltic States
heavy metals in mosses closely correlate to atmos-
pheric deposition (Vargha et al., 2002). Elevated
heavy metal contents decrease the number of wa-
ter bear species and of specimens, and abundance
of tardigrada strongly depends on air pollution
(Vargha et al., 2002). e moss-dwelling fauna
could be a suciently sensitive tool for measuring
the ecological consequences of pollution on the
soil biota (Peluo et al., 2006).
Investigations of terrestrial tardigrades in the
Baltic States
e investigation of tardigrades in the Baltic States
is insucient. Two eutardigrade species groups:
Paramacrobiotus richtersi and Macrobiotus hu-
felandi were recorded in Latvia (Ziemelis et al.,
2012). Two species of genus Isohypsibius: Eremo-
biotus alicatai (Binda, 1969) and Isohypsibius mar-
cellinoi (Binda, Pilato, 1971) were found in Estonia
(Zawierucha, Kaźmierski, 2012). Little is known
about tardigrades in Lithuania. Two genera: Mac-
robiotus sp. and Ramazzottius sp. have been re-
ported in Lithuania two years ago (Šatkauskienė,
Vosyliūtė, 2010) and eight genera of tardigrades
belonging to four families of eutardigrades have
been found in Lithuania last year (Šatkauskienė,
unpublished data, 12th International Symposium
on Tardigrada, 2012).
CONCLUSIONS
Tardigrada are micrometazoans organisms with
a cryptobiotic ability to survive in unfavourable
environmental conditions. However, information
of many aspects of their biology remain unclear.
Irrespective of the most recent molecular investi-
gations, phylogenetic position of these organisms
still remains at the level of controversy. Data of
the tardigrada relation with habitat type, sub-
strate specicity and community ecology are not
comprehensive. Little is known about their sexual
dimorphism, sexual behaviour and gametogene-
sis. e tardigrades belonging to freshwater and
marine species are especially scarcely described.
Despite of the fact that they are common in moss,
lichens and soil, the available information on tar-
digrada in Lithuania so far is very sparse.
Received 30 October 2012
Accepted 2 December 2012
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SCHWÄGR Latvijas Universitātes 70 zinātniskā
konference Bioloăijas sekcija, Zooloăijas un
dzīvnieku ekoloăijas apakšsekcija; 2012.
Ingrida Šatkauskienė
BALTIJOS ŠALIŲ LĖTŪNAI
Santrauka
Straipsnyje apžvelgiama viena mikroskopinių daugia-
ląsčių organizmų grupė – lėtūnai (Tardigrada), išplitę
įvairioje aplinkoje: samanose, kerpėse, dirvožemy-
je, gėlame ir jūriniame vandenyje. Dėl kriptobiotinių
bio loginių savybių ir jų pritaikymo lėtūnai pastaruoju
metu sulaukia nemažai pasaulio mokslininkų dėmesio.
Straipsnyje pateikiami kelerių pastarųjų metų duome-
nys apie lėtūnų paplitimą, taksonomiją ir logeniją, ap-
tariami kai kurie biologijos, dauginimosi ir ekologijos
ypatumai. Pateikiama informacija apie lėtūnų ištyrimą
Baltijos šalyse.
Raktažodžiai: lėtūnai, anhidrobiozė, kriptobiozė,
gėlavandeniai, eutardigrada, heterotardigrada
