Tardigrada Introductory article

Jonathan C Wright, Pomona College, Claremont, California, USA Article Contents

. Basic Design
The Tardigrada comprise a phylum of about 800 described species of minute aquatic . Diversity and Life Styles
animals, showing clear affinities with the arthropods. Many inhabit interstitial or temporary . Cryptobiosis
water bodies, surviving periods of drying by cryptobiosis. . Fossil History and Phylogeny

doi: 10.1038/npg.els.0004140
Basic Design
The essential features of a tardigrade are shown in Figure 1.
Most distinctive are the cylindrical, segmented trunk, usu- interconnecting four large segmental ganglia. These inner-
ally 100–1000 mm in length, and the four pairs of squat, vate the corresponding limbs and muscle groups. The name
‘lobopodial’ limbs bearing claws, the last pair of limbs be- tardigrade is derived from the Latin tardus (slow) and
ing terminal. There is a complex mouthpart apparatus gradus (step) and refers to the lumbering, bear-like gait of
comprising a buccal tube, a pair of piercing stylets and these animals; they are sometimes named ‘water bears’.
associated salivary glands and a tri-radiate muscular phar-
ynx. The pharynx opens into a large midgut, followed by a
shorter hindgut. Opening into the hindgut are three Ma-
lpighian tubules that probably serve in ionoregulation and
excretion, and the single dorsal gonad. The epidermis is
overlain with a flexible chitinous cuticle. Between the
alimentary tract and the epidermis is a spacious haemocoel
that contains large numbers of spherical haemocytes,
approximately 8 mm in diameter. See also: Chitin
The tardigrade nervous system shows a typical proto-
stome pattern. The brain consists of dorsal and paired
ventral ganglia, and is followed by paired ventral cords

Figure 1 Representative Tardigrada. (a) Echiniscus testudo, a common

and cosmopolitan heterotardigrade, showing the buccal sensilla and
thickened cuticular plates with projecting filaments. Length 250–400 mm.
(b) Macrobiotus richtersi, a large eutardigrade (600–1000 mm in length).
Note the curved stylets, wide buccal tube and bulbous pharynx with
masticatory placoids. Figure 2 Claw types of tardigrade genera.

ENCYCLOPEDIA OF LIFE SCIENCES & 2005, John Wiley & Sons, Ltd. www.els.net 1
 Tardigrada
The ‘rolling’ gait arises from the locomotor rhythm in
which opposite and adjacent limbs move 1808 out of phase.
Tardigrade muscles comprise individual cells that originate
and insert at discrete points on the cuticle and work against
the hydrostatic pressure of the haemocoel to bring about
locomotion and shape change. The muscle fibre ultra-
structure is intermediate between smooth and striated
types and resembles that of onychophorans. See also:
Onychophora (velvet worms)
Diversity and Life Styles
Two classes of tardigrades are recognized: the Heterotar-
digrada, which possess a generalized claw structure, ce-
phalic sensilla and often dorsal cuticular plates; and the
Eutardigrada, which show simplified cuticular sensilla and
always possess paired claws. Heterotardigrades include a
marine order, Arthrotardigrada, and a predominantly
freshwater/meiofaunal order, Echiniscoidea. The Eutar-
digrada chiefly inhabit freshwater/meiofaunal biotopes.
Specific genera are most easily distinguished by details of
the claws and buccopharyngeal apparatus; examples are
illustrated in Figures 2 and 3.
Most tardigrades inhabit interstitial water. Habitats in-
clude coastal sands (Batillipes, Orzeliscus), marine rock
crevices or barnacle shells (Echiniscoides), soil water (Mac-
robiotus, Hypsibius), and lichens and moss cushions
(diverse Echiniscoidea and Eutardigrada). A few species
such as Macrobiotus dispar inhabit lakes and rivers. Mosses
and lichens frequently support large populations of
Echiniscus spp. and several eutardigrade genera. Most tar-
digrades feed on algae and plant cells, piercing tissues with
the protracted stylets and withdrawing intact cells or cy-
toplasm with the pumping pharynx. Some species such as
Figure 3 Morphological variation in the buccopharyngeal complex of tardigrade genera.
2
the cosmopolitan Macrobiotus richtersi, M. hufelandi and
Hypsibius prosostomus are facultative carnivores and
may attack other tardigrades, rotifers and nematodes;
Milnesium tardigradum appears to be exclusively carnivo-
rous. See also: Nematoda (roundworms); Rotifera
Reproduction peaks in the summer months, but contin-
ues throughout the year in warmer latitudes. Tardigrades
have separate sexes, although males are generally rare. The
females reproduce mostly by diploid parthenogenesis. A
typical brood size is 3–15 eggs, exceptionally over 20, and
these are often deposited inside the moulted cuticle. The
eggs are frequently ornamented with projecting aeropyles,
which open into a mesh-like chorion; this probably serves
as a respiratory plastron. Meiotic (haploid) eggs are pro-
duced seasonally in some populations, but it is not known
what factors control the switch between mictic (sexual) and
amictic (parthenogenetic) generations. Growth involves
periodic shedding of the cuticle (ecdysis) and continues
throughout life. Prior to ecdysis, the cuticular buccal ap-
paratus is shed, producing a nonfeeding simplex stage. The
new buccal tube and stylets are secreted by the salivary
glands and smaller ‘claw glands’ secrete new claws.
Cryptobiosis
Tardigrades are able to inhabit the ephemeral interstitial
water of mosses and lichens owing to cryptobiosis. This
extraordinary process enables the animal’s tissues to sur-
vive complete loss of liquid water, although some ‘bound’
water remains associated with macromolecules even at ex-
tremely low water potentials. Hazards of dehydration in-
clude intracellular concentration of electrolytes, protein
denaturation, and loss of the hydrophobic–hydrophilic
orienting forces that maintain thermodynamic stability of

Figure 4 Scanning electron micrographs of Hypsibius (Rammazottius)
oberhaeuseri during desiccation and entry into cryptobiosis: (a) partially
contracted; (b) tun (dorsal); (c) tun (ventral). Length of tun approximately
120 mm.
membrane phospholipid bilayers. Cryptobiotic species re-
place electrolytes with compatible osmolytes that serve the
additional function of preserving macromolecular struc-
ture. The most common of these ‘membrane protectants’
Tardigrada
are sugars such as trehalose and mannose, and various
polyols, particularly glycerol. As the moss cushion dries
and water potential declines, tardigrades contract into a
barrel-like tun (see Figure 4) and drying of the cuticle in-
itiates an abrupt decline in permeability. Thus protected
from rapid desiccation, the tardigrade begins a rapid syn-
thesis and mobilization of protectants that stabilize pro-
teins and substitute for membrane-associated water over
the succeeding hours.
Water is the essential solvent for biochemical pathways,
and cryptobiotic organisms in advanced dehydration show
a complete cessation of metabolism. Correlated with this is
a remarkable decline in senescence: tardigrades have been
revived from moss samples dried for over 10 years, and
cryptobiotes protected from oxidation by anaerobic con-
ditions or low temperatures may survive indefinitely.
Many damaging effects of physical or chemical extremes
arise from effects on water, aqueous solute systems and
metabolic regulation, and are ameliorated by drying. Ex-
amples are susceptibility to heating, freezing, organic sol-
vents, anoxia and radiation. The same sugars and polyols
that serve as membrane protectants also protect tissues
against freeze-dehydration and function independently as
antifreezes. High concentrations of trehalose and glycerol
allow some arctic tardigrades to supercool indefinitely
without prior dehydration, avoiding intracellular freezing
and resultant ice damage. This process is referred to as
cryobiosis and is a distinct category of cryptobiosis from
dehydration-induced cryptobiosis or anhydrobiosis.
See also: Water: structure and properties
Both eggs and adults of most ‘terrestrial’ or meiofaunal
tardigrades can exploit cryptobiosis. They share this ca-
pacity with bdelloid rotifers, several protozoans and nem-
atodes, all of which frequently occur with tardigrades in
simple meiofaunal communities. Many other organisms
possess a capacity for cryptobiosis in specific life stages,
including fungal spores, bacteria, pollen grains, seeds and
some insect eggs and larvae.
Freshwater and soil tardigrades may undergo seasonal
encystation in response to an unfavourable chemical en-
vironment. This represents another, distinct form of dor-
mancy. Cyst formation involves contraction of the animal
within the moulted cuticle and secretion of a protective,
heavily tanned cyst cuticle; this is shed at excystation. Cysts
show reduced metabolism and modest desiccation toler-
ance, but details of their physiology are poorly known.
Fossil History and Phylogeny
Two clear tardigrades have been found: single specimens of
a eutardigrade and heterotardigrade from Cretaceous am-
ber. However, recent fossil microarthropods from the
Middle Cambrian of Siberia include a possible tardigrade.
If verified, this would push the origins of the phylum back
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 Tardigrada

Table 1 Tardigrade characters and their phylogenetic implications

Protostome Arthropod/Spiralian Derived characters
Paired, ventral nerve cords Metameric segmentation Small size/eutely
Spiral cleavage a-Chitin procuticle Tri-radiate pharynx
Embryonic protocoely Paired limbs per segment Buccal/stylet complex
Schizocoely (?) Haemocoel Cryptobiosis
rRNA sequence homology Malpighian tubules
Brain/CNS structure

to at least 520 million years ago. Unfortunately, the fossils
in question are already miniaturized animals and give little
clue as to the wider affinities of tardigrades. Their closest
relatives among Palaeozoic fossils are probably the lob-
opodial arthropods from the Cambrian deposits in
Chengjiang, China and the Burgess Shale, British Colum-
bia. These include the many-legged marine Burgessocha-
eta, Aysheaia, Luolishania and Xenusion, which bear
superficial resemblance to onychophorans. Although these
indicate that lobopodial arthropods were widespread dur-
ing the Cambrian, they again provide no information on
when tardigrades first evolved. In the absence of additional
fossil evidence, we depend on comparative studies of extant
species to understand tardigrade phylogeny. See also:
Arthropoda (arthropods); Burgess Shale; Fossil record:
quality
Several workers have proposed affinities between tardi-
grades and the ‘aschelminth’ phyla based on ultrastruc-
tural details of the gut and pharynx, and their capacity for
cryptobiosis. Proposed affinities with aschelminthes are
mostly superficial similarities that fail to support homol-
ogy under closer scrutiny. Cryptobiosis might appear a
compelling phylogenetic character in view of its evident
complexity, but it occurs in all five kingdoms (Prokaryota,
Protista, Fungi, Animalia, Plantae) and several animal
phyla; it is thus of doubtful value as a phylogenetic marker.
More seriously, perhaps, proponents of aschelminth affin-
ities ignore the clear protostome traits seen in tardigrade
embryology and in the nervous system. The most compre-
hensive molecular analyses based on 18S rRNA sequence
data support the existence of a Tardigrada–Arthropoda
clade and do not indicate close relationships with the asc-
helminth phyla. Several features of tardigrades represent
probable consequences of miniaturization and adaptation
to an interstitial habit, including eutely and the lack of
excretory organs in heterotardigrades; this probably ex-
plains some convergent similarities with aschelminthes.
Selected examples of tardigrade characters and their
phylogenetic implications are listed in Table 1. See also:
Cladistics; Molecular phylogeny reconstruction
Presently we cannot say very much about the phylogenetic
position of tardigrades within the Arthropoda. Molecular
evidence, comparative embryology and ultrastructural
details of the cuticle and spermatozoa do not support clear
relationships with the main euarthropod lineages (Crust-
acea, Tracheata, Chelicerata). It seems most reasonable to
classify tardigrades, along with the onychophorans, as lob-
opodial arthropods and sister taxa to the Euarthropoda. If
the Arthropoda is to retain phylum status, the Tardigrada
and Onychophora should therefore be ranked as subphyla.
See also: Chelicerata (arachnids, including spiders, mites
and scorpions); Crustacea (crustaceans); Onychophora
(velvet worms)
The systematics of the Tardigrada were initially laid out
by E. Marcus, who named the modern classes Heterotar-
digrada and Eutardigrada. While the taxonomic charac-
ters outlined above provide the basis for a thorough
systematic breakdown of orders and families, more basal
relationships are speculative. Heterotardigrades are gen-
erally treated as the more primitive class on account of their
diversity in marine habitats. However, marine eutardi-
grades are known. Whether the Eutardigrada are the more
derived group, and if so where they arose within the He-
terotardigrada, are questions that should become clearer
with accumulating molecular evidence.
Further Reading
Bertolani R (1987) Biology of Tardigrades. Proceedings of the 4th In-
ternational Symposium on Tardigrades. Selected Symposia and Mon-
ographs I. Modena: Mucchi Editore, Collana U.Z.I.
Dastych H (1988) The Tardigrada of Poland. Monografie Fauny Polski
16: 1–255.
Dewel RA and Dewel WC (1996) The brain of Echiniscus viridissimus
Peterfi, 1956 (Heterotardigrada): a key to understanding the phylo-
genetic position of the tardigrades and the evolution of the arthropod
head. Zoological Journal of the Linnean Society 116: 35–49.
Garey JR, Krotec M, Nelson DR and Brooks J (1996) Molecular anal-
ysis supports a tardigrade–arthropod association. Invertebrate Biol-
ogy 115: 79–88.
Giribaret G, Carranza S, Baguna J, Riutort M and Ribera C (1996) First
molecular evidence for a Tardigrada–Arthropoda clade. Molecular
Biology and Evolution 13: 76–84.
Higgins RP (ed.) (1975) Proceedings on the First International Symposium
on Tardigrades. Memorie dell’ Istituto Italiano di Idrobiologia 32
(Sppl.): 1–469.
Kinchin IM (1994) The Biology of Tardigrades. London: Portland Press.
Marcus E (1929) Tardigrada. In: Bronn HG (ed.) Klassen et Ordnungen
des Tierreichs 5, section 4(3), pp. 1–608.

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Morgan CI and King PE (1976) British Tardigrades. Synopses of the Brit-
ish Fauna No. 9, Linnean Society of London. London: Academic Press.
Nelson DR (1982) Proceedings of the 3rd International Symposium on Tar-
digrades, Johnson City, TN, 1980. East Tennessee State University Press.
Ramazzotti G and Maucci W (1983) Il Phylum Tardigrada (III edizione
riveduta e aggiornata). Memorie dell’ Istituto Italiano di Idrobiologia
41: 1–1012.
Tardigrada
Weglarska B (1979) Proceedings of the Second International Symposium
on Tardigrades. Zeszyty naukowe Uniwersytetu Jagiellonskiego, Prace
Zoologiczne 25: 1–197.
Wright JC, Westh P and Ramlov H (1992) Cryptobiosis in Tardigrada.
Biological Reviews of the Cambridge Philosophical Society 67:
1–29.