Sponges, Flatworms and Nematodes in Temporary Waters

Sponges. Sponges, although fundamentally a marine group of simple multicellular animals, are nevertheless also quite well represented in a variety of freshwater habitats, including temporary waters. In permanent waters, their natural life cycle includes a dormancy phase, typically during winter. At this time, the active tissues of the sponge body become transformed into gemmules, which represent regression of cells into masses that then become surrounded by a protective coat comprising collagen layers embedded with spicules (Frost 1991). Dormancy seems to be initiated by a number of factors, including changes in water temperature, declining water level, or increasing environmental stress. Species living in tropical regions enter dormancy prior to high summer temperatures, and this is also the case for temporary water forms. Gemmules are particularly resistant to water loss and are able to withstand passive dispersal episodes to other habitats. Both properties are well suited to living in temporary waters. Gemmule hatching seems to be primarily cued by rehydration and a return to normal water temperatures, although photoperiod may also be involved. In some species, the gemmules undergo a true diapause which may add safeguards to prevent premature hatching under temporarily improved environmental conditions (Simpson and Fell 1974).

The role of sponges in freshwater systems is poorly known, although they are believed to be a relatively minor component of the benthic community. However, a study of Spongilla lacustris in Mud Pond, New Hampshire, showed maximum biomass to be over 3.5 g dry weight m~². At this density, the sponge population would, in theory, have been capable of filtering the entire volume of water in the pond every seven days, and, in the process, could have removed most of the bacteria and phytoplankton from the water column (Frost 1978). Similarly, Lake et al. (1989) found Radio- spongilla sceptroides to be a 'conspicuous' component of the fauna of an intermittent pond near Victoria, Australia, where it grew in masses up to 8 cm across on the stems of dead terrestrial vegetation. Clearly then, under certain circumstances sponges can be significant members of the benthos, although quantitative studies in temporary waters are very rare.

Coelenterates. Coelenterates are another group considered to be of minor importance in most freshwaters. Again, they have clear saltwater origins, and are represented in freshwaters by only a few forms whose ecology is poorly understood. The hydras are perhaps the best recognized, represented by simple, solitary polyps, and are often found in temporary ponds or slow- flowing streams. They exhibit both asexual (budding) and sexual reproduction, with the latter producing fertilized eggs surrounded by a thecal coat. The latter appear to have some resistance to adverse environmental conditions. Craspedacusta and Limnocodium are freshwater genera in which the dominant form is a medusa which is budded off from minute, larval polyps ('microhydra'). Craspe- dacusta is known to inhabit shallow pools in the Yang-tse River valley, China, where it is subject to large fluctuations in water level and temperature. Severe temperature changes result in the polyp contracting into a cellular ball which becomes encased in a protective chitin-like membrane (Slobokin and Bossert 1991). Interestingly, mass release of the hydra Chlorohydra viridissima has been tried as a possible control mechanism for mosquito larvae in temporary ponds in California, but with limited success (Yu et al. 1974).

Flatworms. Micro- and macroturbellarians (triclads) are known to live in temporary ponds and streams as well as in some other extreme aquatic habitats including ponds in the high Arctic, alpine meltwater ponds, the leaves of bromeliads, and on wet moss and leaves at water margins (Kenk 1944; Kolasa 1991). However, in general, turbellarians tend to get short shrift in ecological studies, although they clearly are often a component of the biota of temporary waters. Frequently, they are listed as unidentified, and species richness typically seems low (e.g. a single species of Dugesia from an intermittent prairie stream in Kansas, Fritz and Dodds (2002); unidentified Rhabdocoela from a temporary pond in central Italy, Bazzanti et al. (1996); unidentified 'Turbellaria' from ephemeral pans in South Africa, Meintjes (1996)), although occasionally it is higher (e.g. unidentified Neorhabdocoela and Typhlopla- nidae, together with Rhynchodemus cf. sylvaticus from Espolla Pond, Spain, Boix et al. (2001); nine species, from six families, from Namibian wetlands, Curtis (1991)).

In a unique review of the triclads of temporary waters in eastern North America, Ball et al. (1981) determined that only two species occurred regularly in this region: Hymanella retenuova and Pha- gocata velata. These authors stated that the typical turbellarian life cycle is simple and without resistant stages; moreover adults are fragile and susceptible to high temperatures and desiccation. P. velata has become adapted to withstand desiccation by a modification of its asexual cycle in which adults undergo multiple fission at unfavourable times followed by each fragment secreting a layer of slime which hardens into a resistant cyst. The same behaviour has been observed in Phagocata fawcetti, an inhabitant of intermittent streams in California. Hymanella retenuova, which appears to be almost entirely restricted to vernal ponds, does not reproduce asexually, however adults are capable of producing egg cocoons that are thick- shelled and capable of resisting drought.

Densities of both micro- and macroturbellarians may be high. For example, Collins and Washino (1979) recorded more than 1,000 individuals m~² of Mesostoma lingua in Californian rice fields. At such high densities, turbellarians have been cited as both regulating the population dynamics of zooplankton in ponds (Maly et al. 1980), and engaging in intense predation on other turbel- larians (e.g. Dalyellia have been observed to consume Mesostoma and Rhynchomesostoma in temporary pools; Heitkamp (1982)). As a result, some microturbellarians (Typhoplanidae) have been explored as a means of reducing populations of Culex tarsalis larvae in ricefields in California (Case and Washino 1979). Mass release of Dugesia dorocephala has also been tried (Tsai and Legner 1977).

Gastrotrichs. The gastrotrichs represent a phylum of pseudo- coelomate animals (aschelminthes) closely allied to nematode worms. They have both marine and freshwater representatives, although the latter are understudied. Freshwater species live in sediments and in slimy coatings on submerged stones, vegetation, and twigs. They may occur at very high densities (10,000-100,000 m~²) yet their ecological roles are unclear—although they are known to feed on protozoans, algae, bacteria, and fine particulate detritus. They have been recorded from temporary ponds and boggy pools in Poland (Kisielewska 1982; Szkutnik 1986). It is likely that they survive drought in one of the two types of parthenogenetically produced egg: opsiblastic eggs are thick-shelled and are highly resistant to freezing and drying, they also seem to be the principal dispersal phase (Strayer and Hummon 1991). Smock (1999) reported that specimens of Chaetonotus appeared within 3 days of flooding of floodplain soils in the southeastern United States.

Nematodes. Nematodes belong to the largest of the pseudo- coelomate phyla, comprising about 80,000 described species, although some authorities believe that there are upwards of 1 million species yet to be described. There are both free-living and parasitic species, the former being found in the sea, in freshwater, and in the soil, often in huge numbers. Some nematode species are known to occupy very specific niches; for example, hotsprings, meltwater pools on glaciers, and intermittently soaked felt beermats in German pubs. Many species are renowned for withstanding severe environmental conditions, and some have survived immersion in liquid nitrogen. Many live in environments with very low oxygen tensions (e.g. internal parasites and those that live in anoxic muds), yet they are able to maintain their body functions. Under extreme stress, they may enter cryptobiosis, a trait shared by many other lower invertebrates (e.g. rotifers and tardigrades). The sex ratio has been shown to be influenced by prevailing environmental conditions, such that when food is limited males predominate. However, changes in environmental temperature, ions and carbon dioxide content may produce similar results. Females can contain millions of eggs and can produce them at a rate of up to 200,000 per day. Eggs may also be produced as a result of self fertilization (hermaphroditism) or from unfertilized eggs (parthenogenesis). It is clear, then that nematodes possess several physiological and life history traits that would serve them well in temporary waters.

Unfortunately, whereas the category 'Nematoda' frequently shows up in inventories of temporary water communities, it is rare to see species listed. Because nematodes are known to be very abundant in freshwaters (e.g. an estimate of 235,000 individuals of Tobrilus grandipapellatus m~² was made for the benthos of an Austrian alpine lake, in winter; Bretschko (1973)), they are believed to be important consumers of bacteria, fungi, algae, and higher plants (Nicholas 1984). However, their significance in the general economy of freshwater ecosystems is not known (Poinar 1991). By way of comparison, on an estuary mudflat in the United Kingdom, nematode annual production was calculated to be 6.6 gCm^-2yr^-1 (Warwick and Price 1979).

From the limited knowledge of species from temporary waters, the following facts are notable: Bazzanti et al. (1996) recorded Monhystera sp., Dorylaimus stagnalis, Laimydorus centrocercus, and unidentified Dorylaimida as being prominent in a pond in central Italy. Laird (1988) listed free-living nematodes (Adenophorea) as being 'always abundant' in his snow-melt pool in northern Quebec, and 'quite common' in his episodic puddle in Singapore. Taylor et al. (1999) reported nematodes to be common and diverse in shallow wetland ponds on the Atlantic Coastal Plain of North America, however, only one genus, Dorylaimus, was identified. Smock (1999) recorded the genera Miconchus, Labronema, Prismatolaimus, and Dorylaimus from rehydrated riverine floodplain forest soils in Virginia. Also from Virginia, although not strictly from a truly temporary habitat—but from an intermittently freshwater one, Yozzo and Diaz (1999) identified at least 16 species (representing 5 orders and 11 families) from the tidal freshwater marshes of the James River. These included the genera Monhystera, Prismatolaimus, Tylenchus, and Dorylaimus. This latter genus, together with Mesodorylaimus, ?Rhabdolaimus, and a species from the parasitic family Mermithidae have been identified from intermittent ponds in southern Ontario (A.K. Magnusson, Personal communication). For North America, in general, Poinar (1991) lists at least 21 families of freeliving nematodes as containing species which during all or a large part of their life cycles are to be found in freshwaters.

Nematomorphs. Nematomorphs are all aquatic or semiaquatic, with most species living in freshwater. The phylum, which comprises about 320 known species, has a worldwide distribution. Freshwater species live in ponds, lakes, rivers, ditches, and a variety of manmade container habitats. Indeed, the common name 'horsehair worms' was derived both from their general appearance and colour, and the fact that they sometimes live in livestock-watering troughs—where, in past times, superstition had them spontaneously come to life from shed horsehairs. The eggs are laid in long strings in water or very damp soil, with a single female being capable of producing several million eggs. Nematomorph larvae hatch after 15-80 days and each has a pro- trusible proboscis that is covered with spines. After hatching, each larva must seek out and enter a host, either by direct penetration of the host's body wall, or by being eaten. Arthropods seem to be the only viable hosts known, although other animals (leeches, snails, amphibians, fishes, and even humans) may serve as temporary, or 'accidental' hosts. If a larva is eaten by an inappropriate host, the larva may become encysted and thus remains dormant until its host is eaten by a more suitable host. In many instances this does not happen and the life cycle is never completed.

There is still considerable uncertainty about the exact processes involved in host acquisition. After several weeks or months of metamorphosis, the sexually immature, adult worm emerges from the host's body either when the host is near water or during rain. Maturation occurs in the free-living stage, and some species are capable of encysting as adults if suitable environmental conditions are not available. As with several other aschelminth phyla, the Nematomorpha seem to possess traits that pre-adapt them to life in temporary waters. Poinar (1991) lists four genera known from freshwaters in North America, together with another 12 thought likely to occur there but unconfirmed due to lack of study.