Diane R. Nelson

Current Status of the Tardigrada: Evolution and Ecology

Abstract 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.

Young whale sharks, Rhincodon typus, feeding on a copepod bloom near La Paz, Mexico

Seven small (3.2 to 5.2 m total length) whale sharks were observed suction feeding on patches of surface plankton in the Bay of La Paz within 1 km of shore and 2 km N of the phosphate dock at San Juan de la Costa, on 1–2 November 1993. The sharks were photographed and videotaped from the boat and by snorkelers in the water. When actively feeding the shark turned its head from side to side, part of the head was lifted out of the water, and the mouth opened and closed 7 to 28 times per minute (x=17, N=13). These suction gulps were synchronized with the opening and closing of the gill slits. This feeding behavior occurred only in the patchy areas of densely cloudy water, a layer 10 to 30 cm thick at the surface containing an immense concentration of copepods, 95% of which were identified as Acartia clausi. Remoras accompanying the whale sharks also fed on the plankton bloom.

A Family Level Analysis of Tardigrade Phylogeny

In the present study a character data set suitable for cladistic analysis at the family level was developed. A data matrix consisting of 50 morphological characters from 15 families of tardigrades was analyzed by maximum parsimony. Kinorhynchs, loriciferans, and gastrotrichs were used as outgroups. The results agree with the currently accepted hypothesis that Eutardigrada and Heterotardigrada are distinct monophyletic groups. Among the eutardigrades, Eohypsibiidae was found to be a sister group to Macrobiotidae+Hypsibiidae, while Milnesiidae was the basal eutardigrade family. The basal heterotardigrade family was found to be Oreellidae. Echiniscoideans grouped with some traditional Arthrotardigrada (Renaudarctidae, Coronarctidae+Batillipedidae) suggesting that the arthrotardigrades are not monophyletic. The 18S rRNA gene sequence of Batillipes mirus Richters, 1909 and Calohypsibius schusteri Nelson & McGlothlin, 1996 were obtained and their addition to a previously published dataset supports the monophyly of Heterotardigrada and of Parachela versus Apochela within the Eutardigrada.

Chapter 17 – Phylum Tardigrada

A sister group of the Arthropoda, the Tardigrada are micrometazoans that occupy a diversity of niches in freshwater, marine, and terrestrial habitats. Commonly called water bears because of their slow, lumbering gait, these molting lobopods have four pairs of legs, usually terminating in claws. Most are less than 1 mm in length, with a complete digestive tract, a dorsal gonad with one or two gonoducts, and a dorsal lobed brain with a ventral nerve cord and four bilobed ganglia, one per leg-bearing metamere. The body cavity (hemocoel) functions in respiration and circulation. Over 1200 species have been described based primarily on the morphology of the claws and buccal-pharyngeal apparatus. Individuals may be either gonochoric, unisexual, or hermaphroditic, with fertilized or unfertilized eggs deposited either freely or within the shed exuvium. Parthenogenesis occurs frequently in limnic and terrestrial tardigrades, allowing them to colonize new territories by passive dispersal of a single individual. Cryptobiosis (anhydrobiosis, anoxybiosis, cryobiosis, and osmobiosis) and diapause (encystment and resting eggs) occur during the life history. Active adults (surrounded by water) and cryptobiotic adults and eggs are primarily dispersed passively, but some active dispersal can also occur. Due to the characteristic patchy distributions of tardigrade populations, little is known about their population dynamics and trophic relationships. Improved methods for collection, microscopy, culturing, and molecular analyses have been have contributed much to our knowledge of tardigrades.

The Distribution of Tardigrades Upwind and Downwindof a Missouri Coal-Burning Power Plant

Abstract Significant differences occurred in the density of tardigrades, rotifers, and nematodes and the diversity of tardigrades between collecting sites located upwind and downwind from a coal-burning power plant in Missouri. The oak tree species and lichen genera also varied in the two areas. Tardigrade and rotifer densities were greater in upwind sites, whereas nematode density was higher in downwind samples. One tardigrade species (Ramazzottius sp.) was found only at the upwind sites, and one species (Echiniscus sp.) was only in the downwind samples. In contrast, three species (Macrobiotus sp., Minibiotus sp., and Milnesium tardigradum) were found both upwind and downwind but in different densities in the two areas. The study presents baseline data for long-term monitoring of the effects of environmental factors on nematode and rotifer densities as well as tardigrade density and diversity.

Distribution of Tardigrades within a Moss Cushion: Do Tardigrades Migrate in Response to Changing Moisture Conditions?

Abstract The distribution of tardigrades within the layers of the cushion moss Grimmia alpicola Hedwig, 1801 was investigated. The aim of this study was to determine the tardigrade species present within the moss layers during both wet and dry periods and to determine if migration occurred in response to changing moisture conditions. Samples of the moss were removed from concrete caps on brick fence posts before and after rainfall and separated into two sections (top and bottom). The tardigrades from each layer and moisture condition were identified to species. Data for each species were statistically analyzed with a two-way analysis of variance (ANOVA) to compare the numbers of individuals present in the top and bottom layers of the moss under both wet and dry conditions. Five tardigrade species were identified, including two species new to science: Macrobiotus sp. n.; Milnesium tardigradum Doyere, 1840; Echiniscus viridissimus Peterfi, 1956; Echiniscus perviridis Ramazzotti, 1959; and Echiniscus sp. n. The new species will be described in a forthcoming paper. No significant differences were found in the numbers of individuals of four of the five species in each layer within the moss or for each moisture condition. Only one species, E. viridissimus , was significantly more frequent in the top layer of the moss, regardless of moisture condition. Migration within the moss cushion was not detected in any of these five species as a result of changes in moisture conditions. In xeric moss species, it may not be beneficial for tardigrades to migrate to avoid desiccation. Instead, they apparently undergo anhydrobiosis in both the top and bottom layers of the moss cushion.

Ecological Distribution and Community Analysis of Tardigrada from Choccolocco Creek, Alabama

Abstract A seasonal survey of tardigrade populations in the riparian zone of the Choccolocco Creek, Alabama, was undertaken from August 1994 through December 1995. Six sites within the riparian zone were sampled in different portions of the creek. At each site, 3 trees with cryptogams were sampled six times during survey period. From a total of 108 samples, 1,588 tardigrades were extracted and individually mounted on slides in Hoyers medium. The community was dominated (86%) by specimens in the genus Macrobiotus . One species of Echiniscus was new to science and will be described in a separate paper. No significant difference was found between tardigrade occurrence (total number of individuals) and season, moss genera, or tree species. However, there was a significant relationship between the number of tardigrades and site, indicating the need for additional replicate samples. Simpsons and Shannon-Wieners species diversity indices indicated that species richness and evenness were low. Jaccards and Standards community similarity indices suggested that the communities within the riparian zone were dissimilar along Choccolocco Creek.

Chapter 14 – Tardigrada

Publisher Summary Tardigrades are hydrophilous micrometazoans with a bilaterally symmetrical body and four pairs of lobopodous legs usually terminating in claws (and/or digits in some marine species). Tardigrades have commonly been called “water bears” due to their bear-like appearance, legs with claws, and slow lumbering gait. The name “il Tardigrado” (slow-stepper) was introduced to describe the slow, tortoise-like movement of the animal. Thus far, more than 1000 species of tardigrades have been described in two classes (Heterotardigrada and Eutardigrada) from marine, freshwater, and terrestrial habitats (including caves), but the total number of existing species has not been predicted with species richness estimators developed in recent years for biodiversity studies. Generally convex on the dorsal side and flattened on the ventral side, the body is indistinctly divided into a head (cephalic) segment, three trunk segments each bearing a pair of legs, and a caudal segment with the fourth pair of legs directed towards posterior. Although tardigrades range in body length from 50 μm in juveniles to 1200 μm in adults (both excluding the last pair of legs), mature adults average 250–500 μm with very few species exceeding 800 μm. Although some species exhibit color in the gut, storage cells, epidermis, and/or cuticle, most are translucent or whitish (opaque). This chapter describes the anatomy, morphology, physiology, reproduction, life history, phylogeny, evolution, ecology, and taxonomy of tardigrades, with focus on those found in freshwaters of North America.

The Zoogeography of Marine Tardigrada

This monograph describes the global records of marine water bears (Phylum Tardigrada). We provide a comprehensive list of marine tardigrades recorded from around the world, providing an up-to-date taxonomy and a complete bibliography accompanied by geographic co-ordinates, habitat, substrate and biogeographic comments. A link is provided to an on-line interactive map where all occurrences for each species are shown. In total we list 197 taxa and their 2240 records from 39 oceans and seas and 18 Major Fishing Areas (FAO). It is hoped this work will serve as a reference point and background for further zoogeographic and taxonomic studies on marine tardigrades.

Seasonal and Altitudinal Variation in the Distribution and Abundance of Tardigrada on Dugger Mountain, Alabama

Abstract A seasonal survey of the distribution of terrestrial tardigrades on Dugger Mountain, Alabama, was conducted during the time period from April 1997 through April 1998. Cryptogams from five trees ( Quercus alba ), three on north-facing slopes and two on south-facing slopes, were sampled seasonally at three stations (645 m, 410 m, 183 m) along an unnamed tributary of the South Fork of Terrapin Creek. Trees were chosen based on their location outside the riparian zone. Tardigrades were extracted from the samples, mounted individually in Hoyers medium, and identified to species with phase microscopy. Seasonal and altitudinal variations in the distribution of the populations on the north- and south-facing slopes were determined. Present on Dugger Mountain were tardigrades belonging to 12 species ( Macrobiotus cf. areolatus/tonollii, Macrobiotus cf. echinogenitus, Macrobiotus islandicus, Macrobiotus richtersi, Minibiotus intermedius, Milnesium tardigradum, Diphascon pingue, Hypsibius pallidus, Echiniscus cf. arctomys, Echiniscus virginicus, Pseudechiniscus ramazzottii , and Pseudechiniscus suillus ). Due to the small numbers of individuals of each species, the total numbers of tardigrades of all species were pooled. There were no significant differences in the mean number of species or the mean number of all tardigrades per sample at each station (altitude). However, seasonal differences in both abundance and number of species were detected in pooled samples due to the high numbers collected in spring 1997.