Current status of the tardigrada: Evolution and ecology

Integrative and Comparative Biology, Jun 2002 by Nelson, Diane R

Current Status of the Tardigrada: Evolution and Ecology1

SYNopsis. The Tardigrada are bilaterally symmetrical micrometazoans with four pairs of lobopod legs terminating in claws or sucking disks. They occupy a diversity of niches in marine, freshwater, and terrestrial environments throughout the world. Some have a cosmopolitan distribution, while others are endemic. About 900 species have been described thus far, but many more species are expected as additional habitats are investigated. Most are less than 1 mm in body length and are opaque or translucent, exhibiting colors such as brown, green, orange, yellow, red, or pink in the cuticle and/or gut. Marine species are more variable in body shape and overall appearance and generally exhibit low population density with high species diversity. Reproductive modes include sexual reproduction and parthenogenesis, but much remains to be known about development. Tardigrades have a hemocoel-type of fluid-filled body cavity, a complete digestive tract, and a lobed dorsal brain with a ventral nerve cord with fused ganglia. Recent molecular analyses and additional morphological studies of the nervous system have confirmed the phylogenetic position of tardigrades as a sister group of the arthropods. The ability of tardigrades to undergo cryptobiosis has long intrigued scientists. Although tardigrades are active only when surrounded by a film of water, they can enter latent states in response to desiccation (anhydrobiosis), temperature (cryobiosis), low oxygen (anoxybiosis), and salinity changes (osmobiosis). Cryptobiotic states aid in dispersal.

INTRODUCTION

The phylum Tardigrada is often classified as one of the "lesser-known" groups of protostomes. Although much has been learned about these organisms, as evidenced by publications of international symposia (Higgins, 1975; Weglarska, 1979; Nelson, 1982a; Bertolani, 1987a; McInnes and Norman, 1996; Greven, 1999; Kristensen, 2001), the tardigrades present an exceptional opportunity for teaching and research, especially in the areas of development, evolution, and ecology. These micrometazoans may play an important role in the elucidation of metazoan phylogeny, particularly with respect to the evolution of the arthropods. Tardigrades have a ubiquitous distribution, being found in a diversity of niches in terrestrial, freshwater, and marine environments throughout the world, ranging from the abyss in the deep sea to the highest mountains (Ramazzotti and Maucci, 1983; Kinchin, 1994).

General morphology

Small but complex organisms, tardigrades have a bilaterally symmetrical body with four pairs of lobopodous legs usually terminating in claws and/or sucking disks. Mature adults average 250-500 (mu)m, with body lengths ranging from 50 (mu)m in juveniles to over 1,200 lim in adults (although adults of some marine species may be less than 100 (mu)m). They have a complete digestive system and a hemocoel-type of fluidfilled body cavity that functions in circulation and respiration. Reproductive modes include sexual reproduction and parthenogenesis (Bertolani, 1987b; Bertolani and Rebecchi, 1999; Rebecchi and Bertolani, 1988; Rebecchi and Nelson, 1998; Rebecchi et al., 2000), but much remains to be known about development (Nelson, 1982b; Eibye-Jacobsen, 1996/97, 1997). The nervous system consists of a lobed dorsal brain and ventral nerve cord with fused paired ganglia (Dewel and Dewel, 1996; Dewel et al., 1999; Wiederhoft and Greven, 1996, 1999).

Major taxa

Based on morphological characters, the phylum is divided into two major classes: Heterotardigrada and Eutardigrada. A third class, Mesotardigrada, based on a single species, Thermozodium esakii Rahm, is of dubious status. (The type specimens of T. esakii no longer exist and the type locality, a hot spring in Japan, was destroyed in an earthquake. Subsequent searches for the species have been fruitless.)

The class Heterotardigrada is comprised of two orders: Arthrotardigrada and Echiniscoidea. The arthrotardigrades are marine species (with one exception) and usually have a median cirrus on the head and telescopic legs with 4-6 digits (toes) that have complex claws and/or sucking disks; the echiniscoids are primarily terrestrial species with an armored cuticle (having thickened plates), but there are some marine and freshwater unarmored species with telescopic legs bearing up to 13 claws. The class Eutardigrada includes the unarmored orders Apochela (terrestrial) and Parachela (primarily terrestrial and freshwater, with a few marine species); their legs terminate in claws without digits (Schuster et al., 1980). (See Table 1 for classification.)

Taxonomic characters

The two main classes are separated on the basis of taxonomic characters of the claws and/or sucking disks, cuticle, cephalic appendages, buccal apparatus, and reproductive structures. The class Heterotardigrada is characterized by the presence of cephalic, trunk and leg appendages; gonopore separated from anus; Malpighian tubules lacking; placoids consisting of three CaCO^sub 3^ elements or three delicate, bar-shaped cuticular structures (Ramazzotti and Maucci, 1983; Kristensen, 1987). In contrast, the class Eutardigrada has cephalic papillae only in the Apochela (non-homologous to the cephalic appendages in heterotardigrades); gonopore and anus combined to form a cloaca; Malpighian tubules present; placoids consisting of three sets of thickened cuticular structures (Ramazzotti and Maucci, 1983; Schuster et al., 1980; Guidi and Rebecchi, 1996; and others). For a discussion of tardigrade morphology, taxonomic characters, and ecology (primarily terrestrial and freshwater), see Dewel et al., 1993; Dewel and Dewel, 1997; Kinchin, 1994; Nelson, 1982b, 2001; Nelson and Higgins, 1990; Nelson and Marley, 2000; Ramazzotti and Maucci, 1983.