GASTROTRICHA

7

GASTROTRICHA David Strayer

William D. Hummon

Institute of Ecosystem Studies Millbrook, New York 12545

Department of Biological Sciences Ohio University Athens, Ohio 45701

I. Introduction II. Anatomy and Physiology A. External Morphology B. Organ System Function III. Ecology and Evolution A. Diversity and Distribution B. Reproduction and Life History

C. Ecological Interactions D. Evolutionary Relationships IV. Collecting, Rearing, and Preparation for Identification V. Taxonomic Key Literature Cited

I. INTRODUCTION The gastrotrichs are among the most abundant and poorly known of the freshwater invertebrates. Gastrotrichs are nearly ubiquitous in the benthos and periphyton of freshwater habitats, with densities typically in the range of 100,000 – 1,000,000 individuals/m2. Nonetheless, the remarkable life cycle of freshwater gastrotrichs was worked out only recently, and we know almost nothing about how the distribution and abundance of these animals are controlled in nature. The impact of freshwater gastrotrichs on their food resources and on freshwater ecosystems has not yet been investigated. Twelve genera and fewer than 100 species of freshwater gastrotrichs are now known from North America. Because the North American gastrotrich fauna has received so little study, these numbers understate the real diversity of the fauna. Formerly placed in the Aschelminthes or Nemathelminthes, gastrotrichs usually are now considered to constitute a phylum of their own. The evolutionary placement of gastrotrichs is unclear; some authors (e.g., Lorenzen, 1985; Wallace et al., 1996) believe that they are most closely related to nematodes, kinorhynchs, loriciferans, nematomorphs, and priaulids, while others (e.g., Conway Morris, 1993) think that gastrotrichs are more closely related to rotifers and acanthocephalans. Important general references on Ecology and Classification of North American Freshwater Invertebrates. 2nd Edition Copyright © 2001 by Academic Press. All rights of reproduction in any form reserved.

gastrotrichs include Remane (1935 – 1936), Hyman (1951), Voigt (1958), d’Hondt (1971a), Hummon (1982), Ruppert (1988), Schwank (1990), and Kisielewski (1991, 1998). The phylum contains two orders: the Macrodasyida, which consists almost entirely of marine species, and the Chaetonotida, which contains marine, freshwater, and semiterrestrial species. Unless noted otherwise, the information included in this chapter refers to freshwater members of the Chaetonotida. Macrodasyids usually are distinguished from chaetonotids by the presence of pharyngeal pores and more numerous adhesive tubules (Fig. 1). Macrodasyids are common in marine and estuarine sands, but are barely represented in inland freshwaters. Two species of freshwater gastrotrichs have been placed in the Macrodasyida. Ruttner-Kolisko (1955) described an aberrant gastrotrich, Marinellina flagellata (Fig. 1A), from the hyporheic zone of an Austrian river. Unfortunately, she was able to find only two specimens, both of them apparently immature. Because Marinellina has a pair of anterior lateral structures that Ruttner-Kolisko interpreted as adhesive tubules, she placed this species in the Macrodasyida. Remane (1961) rejected the assignment of Marinellina to the macrodasyids and placed it instead in the chaetonotid family Dichaeturidae. Kisielewski (1987) reaffirmed Ruttner-Kolisko’s

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A. External Morphology Gastrotrichs are colorless animals, spindle- or tenpin-shaped, and ventrally flattened (Fig. 2). Freshwater gastrotrichs are 50 – 800 m long. Conspicuous external features include a more or less distinct head, which bears sensory cilia, and a cuticle which, in most species, is ornamented with spines or scales of various shapes. In the most common freshwater family, the Chaetonotidae (as well as in the rare Dichaeturidae and Proichthydiidae), the posterior end of the body is formed into a furca, which contains distal adhesive tubes that allow the animal to attach itself tenaciously to surfaces. In other families, these structures are absent, but the posterior end of the body may bear long spines or sensory bristles. The ventral side of the animal bears longitudinal rows or patches of cilia, which provide the forward-gliding locomotion of the animal.

B. Organ System Function

FIGURE 1

Freshwater macrodasyid gastrotrichs: (A) Marinellina flagellata, and (B) Redudasys fornerise. AT, adhesive tube; and PP, pharyngeal pore. From Ruttner-Kolisko (1955) and Kisielewski (1987).

original placement of the species. An animal similar to Marinellina was just discovered in the hyporheic zone of another Austrian stream (Schmid-Araya and Schmid, 1995); but until it is studied critically, the systematic placement of these enigmatic Austrian gastrotrichs will remain unclear. Kisielewski (1987) discovered an undoubted macrodasyid, Redudasys fornerise (Fig. 1B), from the psammon of a Brazilian reservoir. Additional freshwater macrodasyids probably will be found when appropriate habitats (psammon, hyporheic zone) are explored. The distribution, biology, and evolutionary relationships of any such species will be of great interest.

II. Anatomy and Physiology The following brief account of gastrotrich anatomy is summarized chiefly from Remane (1935 – 1936), Hyman (1951), Hummon (1982), and Boaden (1985), which should be consulted for greater detail.

The digestive system begins with a subterminal mouth, which may be surrounded by a ring of short bristles. Between the mouth and the pharynx lies a cuticular buccal capsule, which is often somewhat protrusible. The muscular pharynx is similar to the nematode pharynx, with a triradiate, Y-shaped lumen. Often, there are anterior and posterior swellings, but these lack the valves characteristic of the pharyngeal bulbs of nematodes. Posterior to the pharynx is an undifferentiated gut, which empties into the anus. The paired reproductive organs lie lateral to the gut in the posterior half of the body. In young animals, large, developing, parthenogenetic eggs are present. As there are no oviducts, the egg is released through a rupture in the ventral body wall. Older animals become hermaphrodites (see below) and bear both sperm sacs and developing sexual (i.e., meiotic) eggs lateral to the gut. An unpaired organ of unknown function, the X-organ, lies posterior to the gonads near the anus. The brain is bilobed, straddling the pharynx. Sensory organs include long cilia and bristles, which presumably are tactile. Balsamo (1980) demonstrated that Lepidodermella squamata is photosensitive, although it does not appear to have distinct multicellular photoreceptors. Gray and Johnson (1970) found evidence of a tactile chemical sense in a marine macrodasyid; it seems probable that freshwater chaetonotids possess similar chemosensory abilities. The excretory system consists of a pair of protonephridia (Brandenburg, 1962) in the anterior mid-

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FIGURE 2 Schematic illustration of a typical chaetonotid gastrotrich showing (A) dorsal view, (B) ventral view, (C) posterior end of a hermaphrodite, showing sexual organs, and (D) egg. AT, adhesive tubes; AN, anus; BR, brain; E, egg; F, furca; G, gut; M, mouth; PH, pharynx; PN, protonephridium; SC, sensory cilia; SS, sperm sac; and X, X-organ. Modified from Remane (1935 – 1936), Voigt (1958), and Kisielewska (1981).

body, which empty through pores on the ventral body surface. There is no circulatory or respiratory system, per se.

III. ECOLOGY AND EVOLUTION A. Diversity and Distribution Gastrotrichs are widely distributed in freshwaters in surface sediments and among vegetation. Some species of the Neogosseidae and Dasydytidae are good swimmers and are occasionally reported from the

plankton of shallow, weedy lakes (e.g., Hutchinson, 1967; Green, 1986; Kisielewski, 1991). However, none of the gastrotrichs has become as truly planktonic as the daphnid cladocerans or ploimate rotifers. Gastrotrichs have been found in a wide range of freshwater and semiterrestrial habitats. They are abundant in most lakes, ponds, and wetlands (Tables I and II). Kisielewski (1981, 1986a) showed that gastrotrich density and species richness are positively correlated with the productivity of the habitat, and several workers have found that gastrotrich density is highest in highly organic sediments (e.g., Strayer, 1985). Apparently, most gastrotrichs live very near the sediment

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David Strayer and William D. Hummon

Number of Species of Gastrotrichs Found in Some Freshwater Habitats.

Habitat

Total

Chaetonotus

European lakesa

18

12

Mirror Lake, NH Ponds, Polandb

20 – 32 21

8 – 20 10

Peat bogs, Polandc Bog pools, Polandd Phragmites mats, Romania Ponds, Brazile Rivers, Brazile

27 24 28 38 22

Other Chaetonotidae

Dasydytidae

Neogosseidae

Source

5

1

0

12 7

0 3

0 1

16 12 16

9 8 7

2 4 5

0 0 0

Preobrajenskaja, 1926; Balsamo, 1981, 1990, Bertolani and Balsamo, 1989 Strayer, 1985 Nesteruk, 1986; Kisielewski, 1986a Kisielewski, 1981 Kisielewska, 1982 Rudescu, 1968

14 5

12 12

10 4

2 1

Kisielewski, 1991 Kisieleswki, 1991

a

Mean of four lakes. Mean of seven ponds. c Mean of four bogs. d Mean of two pools. e Sum of several collecting sites. b

surface in lakes (Fig. 3). Gastrotrichs also are abundant in unpolluted streams, where they inhabit sand bars, sometimes in great numbers (Hummon et al., 1978; Hummon, 1987). Apparently, they are scarce in groundwaters other than the hyporheic zone (RenaudMornant, 1986). Their rarity in underground waters is surprising, because many marine gastrotrichs are interstitial in habit (d’Hondt, 1971a; Renaud-Mornant, 1986), and because the small size and bacterial diet of gastrotrichs would seem to preadapt them to the groundwater habitat. Gastrotrichs are among the few animals commonly found in anaerobic environments (Moore, 1939; Cole, 1955; Strayer, 1985), remaining abundant even during

TABLE II

extended periods (i.e., months) of anoxia. The physiological basis of the anaerobiosis of freshwater gastrotrichs has not yet been studied. It seems likely that some freshwater gastrotrichs possess a sulfide detoxification mechanism similar to that demonstrated for marine gastrotrichs (Powell et al., 1979, 1980) and freshwater nematodes (Nuss, 1984; Nuss and Trimkowski, 1984) to deal with the elevated concentrations of H 2S that often accompany extended anoxia. Little is known of the factors that control the distribution of individual species of gastrotrichs in freshwater. Arguing largely from analogy with marine work (d’Hondt, 1971a), we might expect factors of primary importance to include the granulometry, stability,

Density and Biomass of Gastrotrichs in Some Freshwater Habitats.

Site

Density (No. / m2)

Biomass (mg DM / m2)

Source

Lake Bikcze, Poland Lake Brzeziczno, Poland Lake Piaseczno, Poland Mirror Lake, NH Lake Suviana, Italy Lake Erie, OH Three small ponds, Poland Mississippi River, MN

1,160,000a 920,000 a 910,000 c 130,000 d 57,000 e 50,000 f 1,600,000 – 2,600,000 130,000 – 230,000g

23a,b 30a,b 23b,c 1d — — 25 – 78b —

Nesteruk, 1996 Nesteruk, 1996 Nesteruk, 1996 Strayer, 1985 Madoni, 1989 Evans, 1982 Nesteruk, 1996 Hummon, 1987, and unpublished

a

Littoral zone. Converted from wet mass by multiplying by 0.15. c Mean of three stations. d Lakewide mean. e Mean of two deepwater stations. f Beaches. g Sand bars. b

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FIGURE 3 Vertical distribution of gastrotrichs within the sediments of Lake Brzeziczno, Poland, (dashed line) and Mirror Lake, New Hampshire, (solid line) as a function of depth from the sediment surface. From data of Strayer (1985) and Nesteruk (1991).

packing, and organic content of the sediment, the amount of dissolved oxygen, and the density and composition of communities of microbes and predators. Also, culture work suggests that the inorganic chemistry of the water and the presence of anthropogenic contaminants can exert a strong influence on gastrotrich populations (Hummon, 1974; Faucon and Hummon, 1976; Hummon and Hummon, 1979). Many genera of freshwater gastrotrichs are known to have intercontinental or cosmopolitan distributions. Exceptions include several genera so far known only from Brazil (the macrodasyid Redudasys, the chaetonotids Arenotus and Undula, and the dasydytid Ornamentula); Dichaetura and Marinellina, rare species known only from Europe, and the proichthydiids Proichthydium and Proichthyioides, which have been found only at their type localities in Argentina and Japan, respectively. The geographic distribution of individual species is not well known, because of the primitive state of the species-level taxonomy of freshwater gastrotrichs and the paucity of field studies throughout most of the world. Even in North America, only Arkansas (Davis, 1937), Illinois (Robbins, 1965, 1973; Horlick, 1975), northern Indiana (Pfaltzgraff, 1967), Michigan (Brunson, 1947, 1948, 1950), and eastern Ohio (Craft, 1993) have received even cursory

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surveys of freshwater gastrotrichs. Thus, the 76 species that Schwank (1990) reported from North America probably are a small fraction of North America’s freshwater gastrotrich fauna. Some species have been reported to occur over broad ranges, including in some cases more than one continent (e.g., Kisielewski, 1991). Until further studies are made, such reported intercontinental distributions should be regarded with caution (cf. Frey, 1982; Todaro et al., 1996), especially because “conspecifics” collected from different continents often exhibit marked morphological differences from one another (e.g., Robbins, 1973, Emberton, 1981). Chaetonotus typically dominates gastrotrich faunas everywhere in freshwater, both in terms of numbers of species and numbers of individuals (Table I). Other genera of the Chaetonotidae are common in all kinds of freshwaters, but are usually less abundant than Chaetonotus. The Dasydytidae and Neogosseidae are less widespread than the Chaetonotidae, usually living in weedy, productive waters, where they may, however, become numerically abundant (e.g., Blinn and Green, 1986; Kisielewski, 1981, 1986a; Nesteruk, 1986). Dasydytids and neogosseids also are more abundant and speciose in the tropics than in temperate waters (Table I; Kisielewski 1991). The very rarely seen Dichaeturidae and Proichthydiidae have been collected from cisterns, underground waters, tree holes, and among moss (Remane, 1935 – 1936, Ruttner-Kolisko, 1955; Sudzuki, 1971).

B. Reproduction and Life History Until recently, populations of freshwater gastrotrichs were thought to consist entirely of parthenogenetic females (e.g., Hyman; 1951; Pennak, 1978). However, more detailed recent studies have dispelled this notion, and have revealed a remarkable life cycle among freshwater gastrotrichs (Fig. 4) (Weiss and Levy, 1979; Hummon, 1984a – c, 1986; Levy, 1984). Newly hatched gastrotrichs are relatively large (approximately two-thirds the length of adults — Brunson, 1949) and already contain developing parthenogenetic eggs. These eggs develop rapidly under favorable conditions. At 20°C, the first egg may be laid within a day after the mother hatches. Typically, a total of four parthenogenetic eggs is laid over a 4-day period. Apparently, parthenogenesis is apomictic, so that offspring are genetically identical to their mother. There are two kinds of parthenogenetic eggs. The more common kind, tachyblastic eggs, develop immediately and hatch quickly (within a day of being laid, at 20°C). Occasionally, the final parthenogenetic egg laid by a female is not a tachyblastic egg, but a resting, or opsiblastic, egg. Opsiblastic eggs are thick-shelled, a

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FIGURE 4

Schematic diagram of the proposed generalized life cycle for freshwater chaetonotid gastrotrichs, based predominately on study of Lepidodermella squamata. Dashed lines show hypothetical events which have not yet been demonstrated. From Levy (1984), after ideas presented by Levy and Weiss (1980), with permission of the authors. OPSI, opsiblastic egg; and TACHY, tachyblastic egg.

little larger than tachyblastic eggs, and are very resistant to freezing and drying (Brunson, 1949). The factors that induce the production of opsiblastic eggs are not well known, although such eggs are often produced by animals in crowded cultures. Opsiblastic eggs are almost always the final egg produced by an animal, even if the total number of eggs is fewer than four. Following the production of parthenogenetic eggs, animals develop into hermaphrodites (Fig. 2C) (Hummon and Hummon, 1983; 1988). During this time, sperm and meiotic sexual eggs are produced, and the X-body grows. These changes occur slowly, over the period of a week after the last parthenogenetic egg is laid. No one has yet observed sperm transfer or fertilization, although Levy and Weiss (Levy and Weiss, 1980; Levy, 1984) reported finding a third kind of egg (the “plaque-bearing egg”) in cultures of Lepidodermella squamata. They suggested that plaque-bearing eggs may be the product of sexual reproduction. Because the sperms are few in number (32 – 64 per animal) and nonmotile, fertilization probably is internal. Animals reared in isolation do not appear to produce fertilized sexual eggs, so cross-fertilization probably is the rule. The absence of ducts associated with the male or female reproductive system makes it difficult to suggest a mechanism of sperm transfer (Hummon 1986, described one bizarre possibility). Probably the

enigmatic X-organ is involved. Much remains to be learned about the postparthenogenetic sexual phase and its importance in nature. The life cycle just described is unique among invertebrates and offers considerable ecological flexibility to gastrotrich populations. The initial parthenogenetic phase allows for explosive population growth under favorable conditions: workers have commonly reported growth rates (r) of 0.1 – 0.5 per day in laboratory cultures (e.g., Hummon, 1974; Faucon and Hummon, 1976; Hummon and Hummon, 1979; Hummon, 1986). Production of parthenogenetic resting eggs (opsiblastic eggs) buffers the population against unfavorable conditions and presumably allows for dispersal among habitats. Finally, the subsequent sexual phase introduces genetic recombination. Sexual reproduction is most likely to occur in populations in which rates of mortality are low enough to allow some gastrotrichs to reach the age required for sexual development.

C. Ecological Interactions Gastrotrichs feed on bacteria, algae, protozoans, detritus, and small inorganic particles. Bacteria probably are of primary importance. Bennett (1979) demonstrated that Lepidodermella squamata readily digested bacteria and found that this gastrotrich would not

7. Gastrotricha

survive in laboratory cultures in the absence of bacteria. He reported that L. squamata could digest the green alga Chlorella as well, but suggested that algae were of secondary importance in gastrotrich diets. Gray and Johnson (1970) showed that the marine macrodasyid Turbanella hyalina could choose among various strains of natural bacteria, apparently on the basis of a tactile chemical sense. Thus, the quality as well as quantity of bacterial populations was important to the gastrotrichs. Freshwater gastrotrichs are most likely capable of similar fine discrimination among bacteria and other prey. Reported predators of gastrotrichs include heliozoan and sarcodine amoebae, cnidarians, and tanypodine midges (Brunson, 1949; Bovee and Cordell, 1971; Moore, 1979), but many other benthic predators presumably feed on gastrotrichs. Nothing is known about the importance of predation in regulating populations of freshwater gastrotrichs or about the quantitative importance of gastrotrichs as a food item for various predators. We have no direct information on what regulates gastrotrich populations in nature. Gastrotrichs are capable of enormous population growth (10 – 50% per day) in laboratory cultures. If potential growth rates are anywhere near this high in nature, as seems likely in some circumstances, then there must be an equally high counterbalancing mortality, perhaps from predation. There are no detailed studies of the population dynamics of freshwater gastrotrichs in nature. The few quantitative studies of the seasonal dynamics of freshwater gastrotrich populations (Fig. 5; see also Nesteruk, 1986) have shown that population densities are usually (but not always) lowest during the winter. We do not know what drives these sea-

FIGURE 5

Seasonal trends in gastrotrich abundance. Left: density (number / cm3) of two species of dasydytids in the surface sediments of a boggy pool (“Complex B”) in Poland: Setopus dubius () and Dasydytes ornatus (). From data of Kisielewska (1982). Right: density (number / cm2) of all gastrotrichs (), an unidentified species (probably of Heterolepidoderma) (), and Lepidodermella triloba () on the gyttja sediments of Mirror Lake, New Hampshire (original). Plotted points are means  s.e. (n  16).

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sonal dynamics, but seasonal changes in water temperature, food supply, and predation pressures are obvious possibilities. Gastrotrichs, along with nematodes and rotifers, are among the most abundant animals in the freshwater benthos, often having densities on the order of 10 – 100 individuals/cm2 ( 100,000 – 1,000,000 individuals/m2) (Table II). However, because there have been no direct measurements of the roles of gastrotrichs in freshwater ecosystems, their importance can only be guessed at. There is only a single, tentative estimate of gastrotrich metabolism in freshwater: Strayer (1985) estimated secondary production and respiration of gastrotrichs in Mirror Lake, New Hampshire, each to be 50 – 100 mg dry mass per square meter per year, which is less than 1% of total production or respiration of the zoobenthic community. This estimate suggests that gastrotrich metabolism, and processes such as nutrient regeneration that are correlated with metabolism, are of minor importance in freshwater ecosystems. It would be imprudent, however, to dismiss gastrotrichs as quantitatively unimportant to ecosystem functioning without actually measuring gastrotrich activities under defined conditions. The extraordinarily high rates of population turnover and potentially highly selective feeding behavior of gastrotrichs suggest that they may exert a considerable influence on the composition of natural bacterial communities.

D. Evolutionary Relationships The phylogenetic relationships among the various aschelminth groups are not yet clear. Several points of morphological similarity between nematodes and gastrotrichs (summarized by Lorenzen, 1985, and Wallace et al., 1996) suggest that these two groups are allied, but other analyses (Conway Morris, 1993; Garey et al., 1996) have placed gastrotrichs closer to rotifers and even platyhelminthes than to nematodes. Within the Gastrotricha, only the broad outlines of phylogeny have been sketched out. Three major groups of gastrotrichs are widely recognized: the order Macrodasyida and the suborders Multitubulata and Paucitubulata of the order Chaetonotida. The Multitubulata (which includes only the marine Neodasys) exhibit many primitive characteristics and are in some ways intermediate between the Macrodasyida and the Paucitubulata (which contains almost all of the freshwater gastrotrichs). Therefore, Boaden (1985) suggested that modern Macrodasyida and Paucitubulata are descended from a Neodasys-like ancestor. Nevertheless, on the basis of digestive tract ciliature and other characters, we believe that the ancestral

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David Strayer and William D. Hummon

gastrotrich was more likely similar to the dactylopodolid macrodasyids. Evolutionary relationships among the families, genera, and species of freshwater gastrotrichs are still largely unknown because of a paucity of basic morphological, biochemical, and zoogeographical information about most species. An enormous number of species have not even been described, let alone studied. Even in North America, perhaps 75 – 90% of the species of freshwater gastrotrichs are undescribed. The correct systematic placement of some genera (e.g., Dichaetura, Marinellina) will require much additional study. Furthermore, there is growing concern (e.g., Remane, 1935 – 1936; Ruppert, 1977; Kisielewski, 1981, 1987, 1991, 1997; Schwank, 1990) that some of the traditionally defined genera of the Chaetonotidae may be inadequate. Better morphological information and the discovery of species having characters intermediate between genera is leading to a blurring of distinctions between genera such as Chaetonotus, Heterolepidoderma, and Lepidodermella. Further, it is becoming increasingly clear that some of the characters traditionally used to define gastrotrich genera (e.g., adhesive tubes, cuticle ornamentation) are subject to convergent evolution (e.g., Kisielewski, 1991; Balsamo and Fregni, 1995), and so might not reflect common lines of descent. Finally, it seems likely that Ichthydium, which is defined by an absence of cuticular ornamentation, is polyphyletic. In response to these concerns, Schwank (1990) and Kisielewski (1991) erected new genera of chaetontotids and redefined existing genera, but the classification of this group may need to be redone once more complete information becomes available.

IV. COLLECTING, REARING, AND PREPARATION FOR IDENTIFICATION Gastrotrichs may be collected by taking samples of sediments or vegetation. For quantitative work on sediment-dwelling species, small-diameter (2 – 5 cm) cores are preferable. For plant-dwelling forms, quantitative samples probably could be obtained by modifying sampling methods developed for macroinvertebrates (e.g., Downing, 1984; Jackson, 1997) to use very fine mesh and small sample volumes or subsampling. Because living animals are preferable to preserved animals for many purposes, it often is desirable to extract the animals from the sample prior to preservation. If the sample must be preserved immediately, workers recommend narcotizing the animals with 1% MgCl2 for 10 min, then fixing them in 10% formalin with rose bengal (e.g., Hummon, 1981, 1987).

It is difficult to extract or count the gastrotrichs from a sample. Some workers have handpicked or counted animals under a dissecting microscope (e.g., Hummon, 1981, 1987; Evans, 1982; Strayer, 1985), but this procedure is tedious. Density gradient centrifugation (Nichols, 1979; Schwinghamer, 1981) ought to be useful in extracting gastrotrichs from sediment, but has not yet been tested on freshwater gastrotrichs. Nesteruk (1987) found that a modified Baermann funnel was useful for extracting chaetonotids, but not dasydytids, from pond sediments. Sieves should be avoided or used cautiously, because gastrotrichs are too small to be retained quantitatively on even very fine mesh sieves. For example, Hummon (1981) found that a 37-m mesh sieve retained only 31% of the gastrotrichs in a series of samples taken from the upper Mississippi River. For quantitative work, it is important to check the efficiency of whatever extraction or counting method is used, because gastrotrichs are so small and can be easily overlooked (cf. Strayer, 1985, pp. 295 – 296). Living gastrotrichs are preferable to dead gastrotrichs for taxonomic work. Living gastrotrichs often are too active for critical observations to be made, so they must be slowed down. This can be accomplished by gently squeezing the animal (either with a rotocompressor — Spoon, 1978 — or by removing some of the water from beneath a cover slip with a tissue), by placing it in a viscous medium such as methylcellulose, or by narcotizing it. Cocaine was the traditional narcotic of choice (Brunson, 1959), but it is now difficult to obtain for laboratory use. d’Hondt (1967) recommended using MS 222, and we have had very good success with narcotizing gastrotrichs by bleeding 1.8% neosynephrine (available at pharmacies) under the cover slip. Animals may be killed with formalin or fumes of osmium tetroxide (e.g., Brunson, 1950) following narcotization. Osmium tetroxide is a superior fixative, but is dangerous and should be used with extreme care. It is sometimes necessary to examine individual scales, which can be isolated from an animal by bleeding 2% acetic acid under the cover slip. For serious taxonomic work, videomicroscopy of living animals may provide better permanent documentation of species characters than killed specimens or slides. Procedures for culturing gastrotrichs were described by Packard (1936), Brunson (1949), Townes (1968), Hummon (1974), and Bennett (1979). Gastrotrichs have been cultured on 0.1% malted milk, raw egg yolk, wheat grain infusion, baked lettuce infusion, and baker’s yeast. Brunson (1949) recommended that animals be acclimated gradually to culture media when collected from the wild. Hummon (1974) described a procedure for starting individual cultures of known-age

7. Gastrotricha

animals from eggs that may be especially useful for bioassay work.

V. TAXONOMIC KEY It is relatively easy to identify most North American freshwater gastrotrichs to genus and very difficult to identify them to species. Species identification requires a keen eye, careful observation, a cooperative gastrotrich, and some luck, because most of the freshwater gastrotrichs of North America undoubtedly are undescribed. The following works are helpful in species identification: Brunson (1950, 1959), who keyed and illustrated species then known from North American

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freshwaters; Robbins (1965, 1973), who gave additional information and drawings of North American species; d’Hondt (1971b), who gave a key to the species of Lepidodermella and defined three subgenera of Ichthydium; Kisielewski (1981), who made a critical evaluation of the morphological characters that must be measured to describe (or identify) a species; Kisielewski (1986b), who gave a recent treatment of Aspidiophorus; Schwank (1990), who provided illustrated keys (in German) for all known freshwater gastrotrichs worldwide; and Kisielewski (1991), who described many Brazilian species and addressed several important issues in gastrotrich systematics. The following key includes genera of freshwater gastrotrichs known from or likely to be found in North America.

1a.

Animal with at least three pairs of adhesive tubules (one anterior and two posterior) and a pair of pharyngeal pores, body strapshaped (Fig. 1A,B); an almost entirely marine group not yet reported from North American freshwaters.............order Macrodasyida

1b.

Animal lacking adhesive tubules (Fig. 7A– H ) or with one pair (very rarely two pairs) of adhesive tubules posteriorly (Fig. 6A– L), and no pharyngeal pores, body strap-shaped or tenpin-shaped; common and widespread in freshwater ...............order Chaetonotida ...........................................................................................................................................................................................................2

2a (1).

Posterior end of body usually with furca and adhesive tubules; body usually strap-shaped or tenpin-shaped (Fig. 6A-L) ...................3

2b.

Posterior end of body without furca or adhesive tubules, although sometimes bearing spines or pegs; body usually tenpin or bottleshaped (Fig. 7A– H)..........................................................................................................................................................................12

3a (2).

Furca doubly branched; scales and spines sparse or absent (Fig. 6A); a rare genus not yet reported from North America .................... Dichaeturidae, Dichaetura

3b.

Furca singly branched; scales and spines present or absent (Fig. 6B– L); common and widespread .....................................................4

4a (3).

Branches of furca heavy, sickle-shaped, curved, and tapered, not distinctly divided into a cone-shaped basal part and a distal duct; head with long cilia that are not arranged in bundles; head plates absent (Fig. 6B); a rare family not yet reported from North America ................................................................................................................................................................................Proichthydiidae

4b.

Branches of furca usually with a cone-shaped base and a distal adhesive duct; body often with numerous spines or scales; head with cilia that are arranged in bundles; cephalic plates present (Fig. 6C – L); common and widespread ................................Chaetonotidae ...........................................................................................................................................................................................................5

5a (4).

Branches of furca ringed and often very long; body often large and without a distinct neck (Fig. 6C) ..............................Polymerurus

5b.

Branches of furca not ringed (Fig. 6D – L)...........................................................................................................................................6

6a (5).

Dorsal surface of body without spines or scales (except for dorsal sensory bristles or a few scales at the base of the furca (Fig. 6D) ... ...........................................................................................................................................................................................Ichthydium

6b.

Dorsal surface of body with numerous scales or spines (Fig. 6E – L) ...................................................................................................7

7a (6).

Spines or spined scales present and often numerous (Fig. 6E – G, J) ....................................................................................................8

7b.

Spines absent (occasionally a few thin spines are present at the base of the furca) (Fig. 6H,I ,K,L) .....................................................9

8a. (7).

Ventral scales different from dorsal scales; spines of various types (Fig. 6E – G); common and widespread.......................Chaetonotus

8b.

Ventral scales similar to dorsal scales; posterior part of body with several long spines that reach beyond the end of the furca (Fig. 6J); not yet reported from North America .............................................................................................................Lepidochaetus

9a (7).

Furca without adhesive tubes; body markedly tenpin-shaped, with groups of long cilia on the head and posterior part of the body (Fig. 6H); a semiplanktonic genus known only from Brazil ......................................................................................................Undula

9b.

Furca with adhesive tubes; body strap-shaped or tenpin-shaped; without groups of long cilia on head and posterior body (Fig. 6I,K,L) .....................................................................................................................................................................................10

10a (9).

Dorsal surface of body covered with stalked scales (Fig. 6I) ..........................................................................................Aspidiophorus

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FIGURE 6

Genera of freshwater Dichaeturidae, Proichthydiidae, and Chaetonotidae. (A) Dichaetura; (B) Proichthydium; (C) Polymerurus, showing detail of ringed branches of furca; (D) Ichthydium, (E – G) Chaetonotus, showing examples of spination; (H) Undula; (I) Aspidiophorus, with detail of coat of scales and a single scale; (J) Lepidochaetus, in dorsal (left) and ventral (right) views, (K) Heterolepidoderma, with detail of scales; and (L) Lepidodermella, with detail of scales. From Remane (1935 – 1936), Brunson (1950), Hyman (1951), Voigt (1958), Robbins (1965), and Kisielewski (1991).

10b.

Scales on dorsal surface of body unstalked (Fig. 6K,L) .....................................................................................................................11

11a (10).

Scales elongate, with longitudinal keels (Fig. 6K) ...................................................................................................Heterolepidoderma

11b.

Scales not keeled (Fig. 6L)............................................................................................................................................Lepidodermella

12a (2).

Head with club-shaped tentacles (Fig. 7A,B) .............................................Neogosseidae..................................................................13

12b.

Head without club-shaped tentacles (Fig. 7C – H) .......................................Dasydytidae..................................................................14

13a (12).

Posterior end of body with two groups of long spines (Fig. 7A); elements of mouth-ring jointed.........................................Neogossea

13b.

Posterior end of body with single medial group of spines (Fig. 7B); elements of mouth-ring unjointed .............................Kijanebalola

7. Gastrotricha

191

FIGURE 7 Genera of freshwater Neogosseidae and Dasydytidae. (A) Neogossea; (B) Kijanebalola; (C) Stylochaeta; (D) Ornamentula; (E) Anacanthoderma; (F) Setopus; (G) Haltidytes, and (H) Dasydytes. From Brunson (1950), Krivanek and Krivanek (1958), Balsamo (1983), Schwank (1990), and Kisielewski (1991).

14a (12).

Posterior end of body with pair of peglike protuberances (Fig. 7C) ....................................................................................Stylochaeta

14b.

Posterior end of body without peglike protuberances (Fig. 7D – H) ..................................................................................................15

15a (14).

Body enclosed in a “lorica” of large, thick, ornamented scales (Fig. 7D); known only from Brazil..................................Ornamentula

15b.

Scales absent or small and inconspicuous (Fig. 7E – H) .....................................................................................................................16

16a (15).

Head much narrower than body and scarcely wider than neck; lateral spines absent or identical to dorsal spines; pharynx with two bulbs (Fig. 7E); not yet reported from North America ...............................................................................................Anacanthoderma

16b.

Head distinctly wider than neck; body with long lateral spines; pharynx with one bulb or no bulb (Fig. 7F – H) .............................17

17a (16).

Some lateral spines movable and sharply bent basally; posterior end of body rounded, without rear spines (Fig. 7G)..........Haltidytes

17b.

All spines fixed, straight or bent distally; posterior end of body usually with spines (Fig. 7F,H).......................................................18

18a (17).

Lateral spines with 1 – 3 lateral denticles and often terminally bifurcated; spines of uniform thickness from their base to the last lateral denticle; pharynx usually with a distinct posterior bulb (Fig. 7H) .................................................................................Dasydytes

18b.

Lateral spines tapered, with at most one weak lateral denticle and never terminally bifurcated; pharynx without posterior bulb (Fig. 7F) ...................................................................................................................................................................................Setopus

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VI. LITERATURE CITED Balsamo, M. 1980. Spectral sensitivity in a freshwater gastrotrich (Lepidodermella squammatum Dujardin). Experientia 36: 830 – 831. Balsamo, M. 1981. Gastrotrichi della Toscana: il lago di Sibolla. Bolletino del Museo Civico di Storia Naturale Verona 7: 547 – 571. Balsamo, M. 1983. Gastrotrichi (Gastrotricha). Guide per il Riconoscimento delle Specie Animali delle Acque Interne Italiane 20. Consiglio Nazionale delle Ricerche. Balsamo, M., Fregni, E. 1995. Gastrotrichs from interstitial freshwater, with a description of four new species. Hydrobiologia 302:163 – 175. Bennett, L. W. 1979. Experimental analysis of the trophic ecology of Lepidodermella squammata (Gastrotricha:Chaetonotida) in mixed culture. Transactions of the American Microscopical Society 98:254 – 260. Bertolani, R., Balsamo, M. 1989. Tardigradi e Gastrotrichi del Trentino: il Lago di Tovel. Studi Trentini di Scienze Naturali 65:83 – 93. Blinn, D. W., Green, J. 1986. A pump sampler study of microdistribution in Walker Lake, Arizona, USA.: a senescent crater lake. Freshwater Biology 16:175 – 185. Boaden, P. J. S. 1985. Why is a gastrotrich?, in: Conway Morris, S., George, J. D., Gibson, R., Platt, H. M. Eds., The origins and relationships of lower invertebrates. Clarendon Press, Oxford, UK, pp. 248 – 260. Bovee, E. C., Cordell, D. L. 1971. Feeding on gastrotrichs by the heliozoon Actinophrys sol. Transactions of the American Microscopical Society 90:365 – 369. Brandenburg, J. 1962. Elektronenmikroscopische Untersuchungen des Terminalapparates von Chaetonotus sp. (Gastrotrichen) als Beispeil einer Cyrtocyte bei Aschelminthen. Zeitschrift für Zellforschung 57:136 – 144. Brunson, R. B. 1947. Gastrotricha of North America. II. Four new species of Ichthydium from Michigan. Transactions of the Michigan Academy of Science, Arts, and Letters 33:59 – 62. Brunson, R. B. 1948. Chaetonotus tachyneusticus: a new species of gastrotrich from Michigan. Transactions of the American Microscopical Society 67:350 – 351. Brunson, R. B. 1949. The life history and ecology of two North American gastrotrichs. Transactions of the American Microscopical Society 68:1 – 20. Brunson, R. B. 1950. An introduction to the taxonomy of the Gastrotricha with a study of eighteen species from Michigan. Transactions of the American Microscopical Society 69:325 – 352. Brunson, R. B. 1959. Gastrotricha, in: Edmondson, W. T. Ed., Freshwater biology. 2nd ed., Wiley, New York, pp. 406 – 419. Cole, G. A. 1955. An ecological study of the microbenthic fauna of two Minnesota lakes. American Midland Naturalist 53:213 – 230. Conway Morris, S. 1993. The fossil record and the early evolution of the Metazoa. Nature 361:219 – 225. Craft, L. 1993. A taxonomic survey of freshwater gastrotrichs from eastern Ohio. MS thesis, Ohio University, 169 pp. Davis, K. B. 1937. The Gastrotricha (Chaetonotoidea) of Washington County, Arkansas. MA thesis, University of Arkansas, 94 pp. Downing, J. A. 1984. Sampling the benthos of standing waters, in: Downing, J. A., Rigler, F. H. Eds., A manual on methods for the assessment of secondary productivity in freshwaters. 2nd ed., Blackwell Scientific Publications, Oxford, UK, pp. 87–130 Emberton, K. C. 1981. First record of Chaetonotus heideri (Gastrotricha: Chaetonotidae) in North America. Ohio Journal of Science 81:95 – 96.

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7. Gastrotricha brates. Vol. I: Oogenesis, oviposition, and oosorption. Wiley, London, pp. 211 – 221. Hummon, W. D., Hummon, M. R. 1988. Gastrotricha, in: Adiyodi, K. G., Adiyodi, R. G. Eds., Reproductive biology of invertebrates. Vol. III: Accessory sex glands. Oxford and IBH Publishing Company, New Delhi, pp. 81 – 85. Hummon, W. D., Evans, W. A., Hummon, M. R., Doherty, F. G., Wainberg, R. H., Stanley, W. S. 1978. Meiofaunal abundance in sandbars of acid mine polluted, reclaimed, and unpolluted streams in southeastern Ohio, in: Thorp, J. H., Gibbons, J. W. Eds., Energy and environmental stress in aquatic ecosystems. DOE Symposium Series (CONF – 771114). National Technical Information Service, Springfield, VA, pp.188 – 203. Hutchinson, G. E. 1967. A treatise on limnology, Vol 2: Introduction to lake biology and the limnoplankton. Wiley, New York. Hyman, L. H. 1951. The invertebrates: Acanthocephala, Aschelminthes, and Entoprocta: the pseudocoelomate Bilateria. Vol. 3. McGraw-Hill, New York. Jackson, M. J. 1997. Sampling methods for studying macroinvertebrates in the littoral vegetation of shallow lakes. The Broads Authority, Norwich, UK. Kisielewska, G. 1981. Hermaphroditism of freshwater gastrotrichs in natural conditions. Bulletin de l’Académie Polonaise des Sciences, Série des Sciences Biologiques 29:167 – 172. Kisielewska, G. 1982. Gastrotricha of two complexes of peat hags near Siedlce. Fragmenta Faunistica 27:39 – 57. Kisielewski, J. 1981. Gastrotricha from raised and transitional peat bogs in Poland. Monografie Fauny Polski 11:1 – 143. Kisielewski, J. 1986a. Freshwater Gastrotricha of Poland. VII. Gastrotricha of extremely eutrophicated water bodies. Fragmenta Faunistica 30:267 – 295. Kisielewski, J. 1986b. Taxonomic notes on freshwater gastrotrichs of the genus Aspidiophorus Voigt (Gastrotricha: Chaetonotidae), with descriptions of four new species. Fragmenta Faunistica 30:139 – 156. Kisielewski, J. 1987. Two new interesting genera of Gastrotricha (Macrodasyida and Chaetonotida) from the Brazilian freshwater psammon. Hydrobiologia 153:23 – 30. Kisielewski, J. 1991. Inland-water Gastrotricha from Brazil. Annales Zoologici 43 (Suppl 2):1 – 168. Kisielewski, J. 1997. On the subgeneric division of the genus Chaetonotus Ehrenberg (Gastrotricha). Annales Zoologici 46:145 – 151. Kisielewski, J. 1998. Brzuchorzeski (Gastrotricha). Fauna Slodkowodna Polski 31. Polskie Towarzystwo Hydrobiologiczne, Uniwersytet Lodzki. Krivanek, R. C., Krivanek, J. O. 1958. A new and a redescribed species of Neogossea (Gastrotricha) from Louisiana. Transactions of the American Microscopical Society 77:423 – 428. Levy, D. P. 1984. Obligate postparthenogenetic hermaphroditism and other evidence for sexuality in the life cycles of freshwater Gastrotricha. Dissertation, Rutgers University, New Brunswick, NJ. 257 pp. Levy, D. P., Weiss, M. J. 1980. Sperm in the life cycle of the freshwater gastrotrich, Lepidodermella squammata. American Zoologist 20:749 (abstract). Lorenzen, S. 1985. Phylogenetic aspects of pseudocoelomate evolution, in: Conway Morris, S., George, J. D., Gibson, R., Platt, H.M. Eds., The origins and relationships of lower invertebrates. Clarendon Press, Oxford, pp. 210 – 223. Madoni, P. 1989. Community structure of the microzoobenthos in Lake Suviana (Tusco-Emilian Apennines). Bolletino di Zoologia 56:159 – 165. Moore, G. M. 1939. A limnological investigation of the microscopic benthic fauna of Douglas Lake, Michigan. Ecological Monographs 9:537 – 582.

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