Rotifers and Tardigrades in Temporary Waters: Adaptations

Rotifers. Approximately 2,000 species of rotifer have been described, the vast majority of which live in freshwaters. Habitats include lakes, ponds, bogs, streams, rivers, and puddles, but some live on the moisture-covered surfaces of mosses, lichens, tree bark, or in damp soil. In these latter, temporary water, habitats species survive periodic desiccation by secreting a protective layer of gel. Rotifers can reproduce at prodigious rates with up to 40 generations per year being common. Some species undergo a seasonal change in body shape, known as cyclomorphosis, which is associated with temperature changes and/or changes in predation pressure.

Many species produce two types of egg. 'Summer' eggs are diploid and result in only females. In autumn, heavy-shelled, haploid 'winter' eggs are produced that require fertilization before they can develop. In the spring they give rise to partheno- genetic females. Males develop in the population when haploid eggs fail to be fertilized. 'Winter' eggs are also highly drought-resistant, and may remain dormant for as long as 4 years. In a study of the invertebrates of prairie wetland marshes in Minnesota, Hershey et al. (1999) reported that recovery of rotifer populations after drought was more rapid than in insects, as recruitment of the former was from egg banks in the soil, whereas most insects were believed to recruit from nearby permanent water bodies. These authors also found that rotifers, together with cladocerans, were more abundant and species-rich during a regional drought—with abundance being significantly correlated with the Palmer Hydrologic Drought Index for the previous month. Some 35 rotifer taxa were recorded from these wetlands, with 6 genera being common to all sites sampled (Lepadella, Monstyla, Mytilina, Platyias, Testudinella, and Trichocera).

In two English ponds that were freshly dug out after having been dry for 20 and 40 years, respectively, the earliest colonizers, after only a few days, were the rotifers Keratella valga and Brachionus urceolaris (along with cyclopoid cope- pods and Daphnia obtusa) (Pontin 1989). In both ponds, the rotifers rapidly produced large numbers of parthenogenetic females, but males and resting eggs also appeared soon. Herbivorous species were followed by the omnivorous species Asplanchna brightwelli which was observed to prey on K. valga. Initial colonizers persisted in the ponds for several years after, despite the diversification of the fauna—although the time of their appearance shifted. The 20-year-dry pond subsequently developed a greater diversity of species that may have been related to a higher abundance of macrophytes there.

Bonecker and Lansactoha (1996) related changes in the community structure of rotifers in standing and running water sections of the upper Parana River floodplain in Brazil to environmental factors. Densities of the most abundant species were strongly correlated with chlorophyll a, dissolved oxygen, water temperature, and water level. In contrast, rotifer diversity was mainly related to water level, with species groups being associated with different phases of the hydrological cycle. Hydroperiod was also found to be a controlling influence in a survey of 18 temporary ponds in the Donana National Park, southwestern Spain (Fahd et al. 2000). The ponds were divided into 'seasonal', 'intermediate', and 'ephemeral' according to the length of their hydroperiod. The total numbers of rotifer taxa (and also of crustaceans) were highest in the intermediate-hydroperiod ponds (32 and 26 taxa, respectively). However, even the 'ephemeral' ponds supported a comparatively rich rotifer fauna (21 taxa; plus 20 crustacean species) despite their small size and short wet phase.

Alkins-Koo (1989/90) found the colonial rotifer Conochilus mainly in the slower-flowing, deeper sections of two intermittent streams in southwestern Trinidad. In another Caribbean study, Janetzky et al. (1995) surveyed the rotifers of inland waters on Jamaica, including those species found in phytotelmata and gastrotelmata. The former, primarily in bromeliads, are a typical feature of the understory of the Wet Limestone Forests of the Cockpit Country and represent the only persistent waterbodies there. The latter normally hold water only in the rainy season (September-November) and develop water quality characteristics based on water source (direct rainfall or throughfall via vegetation), the nature of debris in the shell, and by materials dissolved from the shells themselves. The survey produced a list of 205 species (179 monogononts and 26 bdelloids), dominated by three genera: Lecane (25%), Cephalodella and Lepadella (10% each). Ten species were exclusive to aquatic microhabitats: six in gastrotelmata (belonging to the genera Cephalodella, Habrotrocha (also known from the northern pitcher plant S. purpurea), Macrotrachela, and Rotaria); three in phytotelmata (Collotheca, Lecane, and Macro- trechela); and one in rock pools (Lecane). Overall, the Jamaican rotifer fauna resembles that of South and Central America.

Tardigrades. These are very small coelomate animals, ranging from 50 pm up to 1.2 mm in length. There are about 600 species which are found in terrestrial, freshwater, and marine habitats. There are four body segments, each bearing a pair of short legs which end in claws. The body is covered by a cuticle which is shed periodically throughout the animal's life, and which may be either smooth, sculptured, and/or armoured. Although the cuticle contains chitin, it has not developed into the rigid exoskeleton typical of arthropods. It is believed that rigidity would prevent anhydrobiosis (dormancy induced by loss of body water), specifically the formation of the 'tun'stage. This form of the animal requires that the body length be reduced to about 50% through loss of water from the tissues, folding of the dorsal intersegmental cuticle, and invagination of the legs (resulting in reduced surface area and volume). During this process, trehalose (a protective, non-reducing sugar) is synthesized. Again, unlike many arthropods, the tardigrade cuticle is permeable, although it has special lipid layers and air-filled spaces which allow the animal to control cuticular transpiration.

In many terrestrial and freshwater species, parthenogenesis is common and, in some species, there appear to be no males. Parthenogenesis is thought to be linked to the development of anhydrobiosis which is rare in marine species. The eggs of terrestrial species are protected by a thick, ornamented shell. The eggs of aquatic tardigrades are either attached singly to suitable substrates or are laid inside the female's recently shed cuticle. There is no larval stage and a small version of the adult animal emerges from the egg after from 5 to 40 days, depending on species and environmental conditions. In most tardigrades, growth is achieved by an increase in cell size rather than in cell number, however mitosis has been observed in some eutardigrades.

Anhydrobiosis represents one of five types of latency identified by Crowe (1975), the others being: encystment, anoxybiosis, cryobiosis, and osmo- biosis. When in one of these states, metabolism, growth, reproduction, and aging are reduced or suspended, and resistance to environmental extremes such as drought, heat, cold, chemicals, and radiation increases (Nelson 1991). For example, tardigrades can tolerate immersion in liquid helium at —272°C, temperatures as high as 340°C, and can also survive exposure to 570,000 roentgens of radiation (1,140 times the lethal dose for humans). Non-marine tardigrades are incredibly resistant to desiccation (doubtless an adaptation to the intermittently wet habitats in which many of them live). Both adult tardigrades and their eggs can enter a state of deep hibernation which can last for at least 100 years. These dormant stages may be dispersed by the wind. Transition from marine to terrestrial environments has been accompanied by a shift from predominantly striated muscle cells in the tardigrade body towards predominantly smooth muscles. Again, this may be related to the development of anhydrobiosis.

Many tardigrades live in moist, semiterrestrial habitats, such as in damp soil and leaf litter, and among lichens, mosses, and liverworts. Occasionally, they are found in temporary waters and in interstitial environments such as the hyporheic zone. Ramazzotti and Maucci (1983) classified moss-dwelling species into three groups: wet, moist, and dry mosses. Wet mosses, such as those found around lake and stream margins, seldom dry completely. These contrast with mosses growing on trees, rocks, roofs, and walls, which frequently dry out and are dependent on rain for rehydration. Echiniscus molluscorum has been found living in the moist faeces of the land snail Bulimulus exilis (Fox and Garcia-Mol 1962).

Few ecological studies exist on tardigrades, as is exemplified by the fact that out of 39 recent studies of regional wetlands in North America (Batzer et al. 1999), only one includes tardigrades in its faunal inventory. Yozzo and Diaz (1999) list the following seven species from tidal freshwater marshes on the James River, Virginia: Isohypsibius saltursus, Macrobiotus richtersii, M. dispar,M.furcatus, M. hufelandii, Hypsibius sp. (Eutardigrada: Macro- biotidae), and Echiniscus sp. (Heterotardigrada: Scutechiniscidae). In a rare study of the population dynamics of two species living in damp roof moss in Wales, Morgan (1977) found population densities of up to 823 individuals g^—1 of moss. Temporal variation in the numbers of both Echiniscus testudo and M. hufelandii appeared to be cyclical and positively correlated with temperature and the number of daylight hours. Further, increases in humidity and rainfall, 10-20 days prior to sampling, produced a decrease in densities, but an increase in the size of individuals. In an attempt to expand on the moss 'wetness/dryness' scale (Petersen 1951) for categorizing moss-dwelling tardigrades, Kathman and Cross (1991) explored correlations with moss species, degree of exposure, and an altitudinal gradient, but none was found. They concluded that species composition was probably related to microenvironmental conditions within individual moss tufts.