© 2002 by The Society for Integrative and Comparative Biology
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Rotifers: Exquisite Metazoans1
1 Department of Biology, Ripon College, Ripon, Wisconsin 54971
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SYNOPSIS |
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TOP
SYNOPSIS
INTRODUCTIONRotifers comprise a modestly sized phylum (
1,850 species) of tiny (ca. 50–2,000 µm), bilaterally symmetrical, eutelic metazoans, traditionally grouped within the pseudocoelomates or Aschelminthes. These saccate to cylindrically shaped protostomes possess three prominent regions (corona, trunk, foot). They are distinguished by a ciliated, anterior corona (used in locomotion and food gathering) and a pharynx equipped with a complex set of jaws. Unfortunately, these generalizations grossly oversimplify a rich and fascinating diversity. Chief among the charms of the study of rotifers are their ecological importance, ease of culture (including chemostat technology), and the fact that much remains unknown about this exquisite phylum. |
INTRODUCTION |
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"The rotifers are the most important soft-bodied invertebrates in the fresh-water plankton."G. Evelyn Hutchinson (1967) A Treatise on Limnology, Vol. II
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INTRODUCTION |
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Rotifers ought to be well known. Being among the first microorganisms seen by children exploring pond life with their new microscope or high schoolers in biology class, rotifers have fascinated people for more than 300 yr, ever since Leeuwenhoek began describing them late in the 17th century (Dobell, 1958
). They are available from biological supply houses or are easily obtained from a variety of freshwater and terrestrial habitats, including soils and the water films on mosses. These factors alone privilege their use in introductory biology courses as a representative of the groups traditionally termed pseudocoelomates or Aschelminthes. Textbooks on invertebrate zoology offer good summaries of the phylum, while advanced treatises provide intriguing details (e.g., Clément and Wurdak, 1991; Nogrady et al., 1993; Wallace and Snell, 2001). Every three years beginning in 1976 the community of rotiferologists meets to exchange ideas; to date nine symposia have been published, mainly in Hydrobiologia. Rotifers have even entered our cultural ethos, being the subject for children's literature (Bayliss, 1912), a cartoon in the news magazine Discover, and artists working with glass (Miner, 1931). However, while some species are well known and easy to culture, our efforts have lagged behind those of many other invertebrate zoologists. In fact, much of what we know about rotifers is based on only a few genera, especially Brachionus, called the "white mouse" of rotifers by Charles King (personal communication) (see also Yúfera, 2001). Here I review some recent trends in rotifer research, offering questions that provide distinct challenges for future work. |
ROTIFERAN BAUPLAN |
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Rotifera is a moderately sized phylum of some 1,850 species (Segers, 2002
) of tiny (ca. 50–2,000 µm), bilaterally symmetrical, eutelic (ca. 1,000 cells), gonochoristic protostomes. They are saccate to cylindrically shaped animals with three prominent regions (corona, trunk, foot) (Fig. 1). Unfortunately, this simple description oversimplifies a rich and fascinating diversity.
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The defining rotiferan feature is an anterior ciliated field, the corona (Fig. 1). In many species, the corona is developed as two concentric rings of cilia (trochus and cingulum) that beat in a metachronous pattern. This action, resulting in an illusion of a rotating wheel, informs the allusion used to conceive the phylum's etymon (L., rota + ferre, wheel-bearers). A second critical feature is a muscular pharynx (mastax) with chitinous jaws (trophi). Trophi are composed of seven articulating pieces which process food in a variety of ways (e.g., grinding, piercing-pumping, grasping) (Fig. 2). In some forms, classification to species may be ascertained based on trophi alone. Challenges—There appears to be homology in the jaws of Rotifera and Gnathostomulida (Rieger and Tyler, 1995
), which extends to Micrognathozoa (Ahlrichs, 1997; Kristensen and Funch, 2000). Can molecular analysis confirm this relationship? (See also the section Phylogenetic quandaries, below.)
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The syncytial integument of rotifers is notable in that it contains an intracytoplasmic lamina (ICL) composed of two filamentous, keratin-like proteins (39K, 47K Daltons), cross-linked by disulfide bonds (Bender and Kleinow, 1988
; Clément and Wurdak, 1991). When major portions of the ICL are thickened the bodywall is somewhat less flexible; such species are called loricate. Species lacking such thickening are called illoricate. Although the ICL has little taxonomic significance, it is synapomorphic with phylum Acanthocephala, indicating a close phylogenetic relationship. CHALLENGES—Rotifers appear to be very different from acanthocephalans. What is the phylogenetic relationship between these taxa? (See also Phylogenetic quandaries.) |
REPRODUCTION |
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Reproductive strategies vary among the classes (Wallace, 1998
; Ricci, 2001). Class Seisonidea is dioecious with gametogenesis taking place by ordinary meiosis. Class Bdelloidea (diploid) reproduces exclusively by ameiotic parthenogenesis. Class Monogononta (haplodiploid) exhibits a cyclical parthenogenesis with the asexual cycle (amictic females) dominating (Fig. 3). Sexual reproduction in monogononts (mixis) occurs only after being triggered by specific environmental signals (e.g., high population density). Mixis results in the production of mictic females which produce haploid eggs or, if fertilized, diploid embryos (resting eggs or cysts). Resting eggs undergo obligatory diapause, eventually hatching as amictic females. Thus, the ecological and reproductive roles of amictic and mictic females differ, and it is of interest to understand the strategies that allot resources to each (Aparici et al., 1998; Serra and King, 1999). CHALLENGES—(1) What is the optimal sex allocation of amicitic vs. mictic females and can published models be tested in natural or laboratory populations (Aparici et al., 1998, 2002; Serra and King, 1999; Ciros-Pérez et al., 2002)? (2) Although sexuality is still believed to be plesiomorphic, for many monogononts sex has never been observed. Has this character been lost in these species, are local environmental signals unable to trigger mixis, or have sexual periods been missed due to infrequent sampling?
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OTHER CHALLENGES—Three other interesting features of the monogonont life cycle await additional study (Fig. 3). (1) Females in some species of Asplanchna, Conochilus, and Sinantherina are capable of producing both diploid (mitosis) and haploid (meiosis) eggs; these so-called amphoteric females can produce males and resting eggs or females and resting eggs. What is the mechanism of this switch in nature? Pseudosexual eggs have been reported in a planktonic species of Keratella, but this may simply be due to the fact that inadequate sampling has missed the brief period of sexuality (Nogrady et al., 1993
). (2) In culture Synchaeta pectinata is capable of producing diapausing amictic eggs along with non-diapausing eggs, with the proportions being controlled by food limitation (Gilbert and Schreiber, 1998). The significance of this phenomenon appears to be a risk-spreading strategy under conditions of low food. Does amictic diapause occur in other species? (3) Males of most species are structurally reduced (dwarfism, progenesis), within a continuum ranging from slightly reduced in Rhinoglena to highly reduced in Asplanchna (Ricci and Melone, 1998; Serra and Snell, 1998). Selection for male dwarfism may be a strategy that maximizes male production with a minimum reproductive cost. Is there a pattern to distribution of male dwarfism in rotifers and is it reflected in their habitats? |
TAXONOMY |
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Simply put, when compared to other freshwater micrometazoans (i.e., cladocerans, copepods) rotifers suffer from a serious lack of taxonomists. In Europe, where the situation has always been better, taxonomic training appears to be healthy, while in North America the number of taxonomists has fallen to a critically low level. In all, what we know about rotifer taxonomy, biogeography, and records of invasions are limited to those places were rotifer workers live or where they have had the opportunity to sample. In practical terms, much of the world, including the U.S., remains aqua incognita for detailed rotifer work. CHALLENGE—How can we increase taxonomic training and study?
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ECOLOGY |
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Rotifers are important components in freshwater ecosystems
Until the 1980s contributions of rotifers to the trophic dynamics of lakes were frequently overlooked. However, although individual biomass is minute, large population size, coupled with high turn-over rates make rotifers an important component of food webs (Herzig, 1987
; Starkweather, 1987; Walz, 1997). Adding to their importance is the fact that rotifers are eaten by invertebrate predators and are also the first food of fish fry, thereby making their energy available to higher trophic levels. While recent work indicates that rotifers are significant components of microplankton community structure, the magnitude of that importance has not been completely explored (Arndt, 1993; Berninger et al., 1993; Rublee, 1998). CHALLENGES—(1) How important are rotifers to microplankton food webs in a variety of habitats? (2) How important are rotifers to the ecology of springs and soils (Pourriot, 1979), interstitial (Wallace and Ricci, 2002), and periphytic habitats (Duggan, 2001)?
Population biology
Examination of annual population cycles of rotifers from a variety of habitats indicates that species abundance can differ markedly from year to year (Herzig, 1987). Unfortunately, even short-term sampling schedules (weekly) can miss the details of population peaks (Berner-Fankhauser, 1987). Thus variability, coupled with difficulties involved in sustaining intensive sampling schedules, makes studying population dynamics difficult. Use of chemostats along with particle-counting technology, however, permits systematic manipulation of experimental conditions, thereby allowing tests of population growth models (Walz, 1993). For example, Boraas et al. (1998) and McNair et al. (1998) offer a model with separate components for eggs (based on age) and free-swimming individuals (based on age-specific biomass). CHALLENGES—(1) How can sampling techniques be improved to assess spatial and temporal variation within populations? (2) Can chemostat models be employed to test interpretations of the dynamics of natural populations?
A miner's canary?
Rotifers have been used in pollution monitoring either as bioindicator species or as part of the saprobic assessment system for some time. The former simply relies on a list of species known to indicate pollution (Mäemets, 1983), while the latter integrates a large number of abiotic and biotic characteristics into a single variable describing the relative level of eutrophication (Sládecek, 1983; Marneffe et al., 1998). In addition, because rotifers are relatively easy to culture and sensitive to pollutants they have become important tools in ecotoxicological testing (ET). In ET, rotifers are exposed according to standardized protocols to compounds with results being reported as LC50s, EC50s, or NOEs (no observed effects) for reproductive and/or behavioral endpoints (ASTM, 1991; Snell and Janssen, 1995). Other work in this field has focused on cellular and enzymatic biomarkers as indicators of sublethal effects (Snell and Janssen, 1995). Recent examination of UV radiation as a factor influencing survival and reproduction of aquatic organisms has provided valuable information on the effects of UV on rotifers (e.g., Leech and Williamson, 2000). This work indicates that there is a wide range in tolerance, with Keratella spp. being among the most tolerant and Asplanchna priodonta among the least. Similarly, Perez-Legaspi and Rico-Martinez (2001) have shown that LC50s varied up to 22 times for three species of Lecane. CHALLENGES—(1) How robust are these testing protocols when only a few species have been used and when LC50s vary widely even among members of the same genus? (2) Is it feasible to use rotifers as models for toxicity screening given the numbers of chemicals that need to be tested? (3) Can rotifers be of practical use as biosensors of environmental degradation or contamination? (4) Is it possible to determine the fate of toxicants and the presence and efficiencies of detoxification systems in rotifers?
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SYSTEM AND ORGANISMAL LEVEL STUDIES |
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Knowledge of neurobiology is meager
Comprising about 25% of the total number of cells in the body, the rotiferan nervous system is simple, consisting of a concentration of ganglia at the anterior end (brain), several additional ganglia serving the mastax, body, and foot, paired ventral neurons, and three sensory organs (mechano-, chemo-, photo-receptors). In addition, many species possess a retrocerebral organ, comprising paired subcerebral glands, an unpaired retrocerebral sac, and ducts leading to the coronal surface. CHALLENGES—(1) What is the function of the retrocerebral organ? (2) Can neuroanatomy provide additional phenetic traits for phylogenetic studies (see below)?
A few neuro-pharmacological investigations have shown that cholinergic systems function in at least 12 species representing six families and that adrenergic and catecholaminergic systems have been observed in other species, including both bdelloids and monogononts (e.g., Nogrady et al., 1993; Kotikova, 1995, 1998). These studies indicate that (1) distribution of neurons in rotifer brains are bilateral with distinct species-specific patterns, (2) bipolar neurons are typical, but that uni- and multipolar neurons also are present in small numbers, and (3) catecholaminergic neurons comprise 5% of the total number of brain cells. CHALLENGE—Are the details of rotifer neuroanatomy and neuophysiology uniform across a wide array of taxa?
Several researchers have studied the effects of environmental stimuli on rotifer behavior including movement (Charoy et al., 1995), feeding (Starkweather, 1987, 1995; Bevington et al., 1995), mating (Snell, 1998), and substratum selection (Wallace, 1980). However, efforts by Joanidopoulos and Marwan (1998) have yielded some extraordinary insights to the relationship between neuroreceptors and behavior. While holding male Asplanchna sieboldi on the tips of microcapillary tubes, these workers stimulated their coronal sensory receptors using the chemical and mechanical stimuli associated with male-female encounters. These stimulations triggered specific male mating responses. CHALLENGE—Will we employ these and other procedures such as microelectrode technology, dye injection, cell labeling, photometry, and video imaging to better characterize rotifer neurobiology?
Aging studies
Use of rotifers as models for aging makes sense as they are eutelic, have short lifespans, and are inexpensive to culture under conditions suitable for life history analysis. However, although the earliest aging work dates from the 1880s, there has never been a consistent effort to examine a variety of species or to systematically test all aging theories using rotifers. Some of the studies that have been done have examined effects of maternal age, pattern of reproduction, photoperiod, and various antioxidants on aging and life history. However, of the dozen or so theories of aging, only four have been examined using rotifers (Enesco, 1993). According to Enesco, the rate of living theory is not substantiated, but there is support for the free radical damage and calcium theories (cf. King, 1983). Based on the fact that chemical signals are known to evoke a variety of life history events in rotifers, Enesco also proposed programmed aging as a plausible model for rotifer aging. In this model, the withdrawal of a reproductive hormone serves as the programmed signal for termination of life. CHALLENGES—(1) Can other theories of aging be examined using rotifers? (2) Is it possible to link aging studies to those of ET (see above)? (2) Given that rotifers are eutelic, have they retained DNA repair enzymes?
Coloniality in rotifers is not understood
Unlike some colonial invertebrates, rotifers do not share energy resources among colony members. Therefore, the fact that colony formation should be found at all is remarkable; intuitively one would expect that their only interactions would be as mates, competitors, or in predator-prey relationships (Wallace and Snell, 2001). Nevertheless, although not a widespread phenomenon, 25 species in all eight genera of family Flosculariidae (microphagous monogononts) form permanent colonies. Further, there appears to be a connection between coloniality and being sessile, for about 70% of colonial taxa (18 species) are sessile (Wallace, 1987). CHALLENGE—How is coloniality linked to the sessile life-style?
Colony size varies considerably from a minimum of two members (Floscularia ringens) to truly gargantuan colonies of >1,000 in certain Lacinularia species. Regardless of size, colonies form by one of three different methods termed allorecruitive, autorecruitive, and geminative (Fig. 4). Coloniality may have three important implications (Wallace and Snell, 2001). (1) Coloniality may improve individual energetics. (2) It may decrease predatory success of tactile and even certain visual predators. (3) Colony formation method implies differences in the genetic relatedness of colony mates. CHALLENGE—The methodologies appear to be available to test these hypotheses, but is it possible to do so?
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Spines are used as foils and in making rapid jumping movements
Spine formation in rotifers has been recognized as a defensive mechanism that reduces predation by tactile predators (Gilbert, 1999
). The classic example is seen in Brachionus calyciflorus. When amictic females of this planktonic monogonont are exposed to a water-soluble factor from the predatory rotifer Asplanchna, the next generation is born with posterolateral outgrowths of the body wall (spines). These spines are extended slightly away from B. calyciflorus when it is disturbed, thus making it more difficult to manipulate and ingest by Asplanchna. While there are other consequences to spine production, it is clear that some spines, whether moveable or not, act as foils frustrating tactile predators. CHALLENGE—What is the mechanism of embryonic induction of spines in B. calyciflorus and other species which form spines by induction?
Not all appendages in rotifers function by directly interfering with predatory attack. Some species possess movable extremities that swing, making wide, arc-like movements (i.e., Filinia, bristles; Hexarthra, setous arms; Polyarthra, paddles). For example, when Polyarthra detects shear disturbances, as might be produced by a predator (copepods) or large suspension feeder (daphnids), it flicks its paddles very rapidly. The results of this behavior are a series of swift jumping (escape) movements which achieve remarkable speeds: ca. 20 mm/sec or >150 body lengths/sec (Gilbert, 1987). CHALLENGE—The mechanics of these jumps appear to be more akin to rowing (i.e., of water striders). What is the biophysics of these remarkable movements?
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GENETICS AND PHYLOGENY |
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Progress in genetics
For many years progress in understanding rotifer genetics was hampered by the fact that no morphological trait had been linked to a specific gene (King, 1977
). However, our knowledge has been greatly advanced through application of several techniques, including cross-mating tests (Rico-Martínez, 1998), combination of allozyme and morphometric techniques (Serra et al., 1998; Gómez, 1998), DNA hybridization (D. Mark Welch and Meselson, 1998), karyotyping (J. Mark Welch and Meselson, 1998), and gene sequencing (Garey et al., 1998; Mark Welch, 2000; Mark Welch and Meselson, 2001). One specific aspect of rotifer genetics that is being untangled is the determination that bdelloids have evolved without sex for tens of millions of years (Mark Welch and Meselson, 2000). Another fundamental question of rotifer phylogeny is whether there are cryptic species present within what otherwise appears to be a solid species. For example, using a region of the mitochondrial cytochrome oxidase subunit I gene, Gómez et al. (2000) have concluded that populations of a brackish water species, Brachionus plicatilis, from the Iberian Peninsula show deep phylogeographic structure. Gómez and her coworkers have concluded that two main lineages probably began to separate early in the Pleistocene. This molecular work has been augmented by classical taxonomy with the description of three species within the B. plicatilis complex (Ciros-Pérez et al. 2001). CHALLENGES—(1) Regardless of progress made in the past 25 yr it is interesting to note that many significant questions articulated 25 yr ago are still largely unanswered: i.e., compare King (1977) to King and Serra (1998). (2) Are cryptic species common within the phylum? (3) What is the genetic system responsible for the switch from asexual to sexual reproduction in monogononts?
Phylogenetic quandaries
Rotifer phylogenetic studies began to catch up to the rest of zoology with application of modern techniques, but this does not mean there is unanimity of thinking on rotifer evolution. Nevertheless, some progress has been made. For example, taxon Digononta has been rejected by both morphologically and molecularly based analyses (Ahlrichs, 1997; Melone et al., 1998; Mark Welch, 2000, 2001). However, the relationship between Rotifera and Acanthocephala has not been resolved. Moreover, the hypotheses regarding the evolutionary relationships of these and other taxa are somewhat chaotic (Fig. 5). These ideas may be summed up as follows: acanthocephalans are a sister-group of Rotifera, sensu stricto (Melone et al., 1998; Nielsen, 2001), Bdelloidea (Lorenzen, 1985; Garey et al., 1998; Garey and Schmidt-Rhaesa, 1998; Winnepenninckx et al., 1998), Seisonidea (Ahlrichs, 1997), or Eurotatoria (Bdelloidea + Monogononta) (Mark Welch, 2000, 2001). In part, this debate rests on some fine points of the way the analyses have been worked. For example, in some morphologically based studies the issue is whether the lemnisci and proboscis of acanthocephalans are homologous to the hypodermic cushions and apical rostrum of bdelloids (Lorenzen, 1985; Ricci, 1998; Nielsen, 2001). Without detailed ultrastructural and development support, it seems premature to proclaim these features to be homologous.
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Molecularly based studies also differ in several ways, and that appears to depend on which genes are analyzed and whether the euryhaline monogonont, Brachionus plicatilis is included. The study of Garey et al. (1998)
, which used two genes (18S rRNA and mt 16S rRNA) and B. plicatilis, yielded a tree in which acanthocephalans cluster as modified bdelloids. However, a study by Mark Welch (2000), which did not include B. plicatilis, and used the hsp82 gene, yielded a tree that placed acanthocephalans as a sister-group to the Eurotatoria. CHALLENGES—(1) Future work needs to include (a) additional taxa (especially from within Rotifera), (b) fresh morphological characters, and (c) more gene sequences. (2) Also unresolved are the phylogenetic positions of Cycloneuralia, Chaetognatha, Gnathostomulida, Cycliophora, and Micrognathozoa (Funch and Kristensen, 1995; Winnepenninckx et al., 1998; Kristensen and Funch, 2000). |
OTHER INTERESTING TOPICS |
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Space does not permit an evaluation of other inviting topics, including physiology, development, morphology, dormancy patterns, biogeography and biodiversity, chemical ecology, and host-parasite relationships. As a group, the bdelloids offer numerous interesting problems, but except for a scant handful of workers, this taxon does not receive the research it deserves (e.g., Ricci, 2001
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PRACTICAL STUDIES AND SOME SPECULATION |
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Wedding knowledge of culture methods and the fact that rotifers are highly nutritious foods for the larvae of marine crustaceans and fish, aquacultural technologies have been producing enormous qualities of rotifers in very large culture systems for more than 30 yr. In this regard, rotifers may be seen as living nutrients (i.e., tiny, free-swimming, food capsules) that may be artificially augmented with highly unsaturated fatty acids and antibiotics, both of which are important to improve survival and growth of the larvae. As a result of these intensive efforts, rotifers provide an important link in the food supply in many countries including China, India, Israel, Japan, Spain and Thailand (e.g., Lubzens et al., 1989
, 2001). While much of this work has concentrated on B. plicatilis, recent efforts with freshwater species in this genus have been undertaken and are expected to grow. CHALLENGE—An important aspect of this practicum is to refine the technology making it more economically feasible for use in developing countries.
One exciting extension of this aquacultural labor is that knowledge gained from commercial enterprises may be adapted to space travel. So far the work is very preliminary, involving only the feasibility of rotifer culture in low- or zero-g conditions (Ricci et al., 1998). The next steps will require development of fully functional micro- or mesocosms and then practical aquaculture systems modeled after extant systems. CHALLENGE—Might rotifers become part of artificial ecosystems onboard spacecraft which are then re-adapted into an intensive aquaculture system for an offworld colony?
Mining the biological world for useful biomolecules currently engages a large research effort. Although this is pure speculation, I suggest that rotifers are a target organism for a similar effort. For example, as a group, rotifers possess trophi adapted to capture and process a wide variety of foods in diverse ways (De Smet, 1998; Kleinow, 1998). Some of these trophi share a striking resemblance to complex tools (forceps) as might be used in surgery (Fig. 1). CHALLENGE—Could certain rotifer trophi serve as models for a new microtechnology?
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CONCLUSIONS |
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This review considers research trends in rotifers and suggests what might be accomplished with additional effort. With that in mind, I offer the same sagacity presented to me over 30 yr ago (Donald Zinn, personal communication). Should you wish to study a group of invertebrates about which little is known, consider rotifers.
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ACKNOWLEDGMENTS |
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I thank Alan Kohn, Doug Light, Tom Nogrady, Elizabeth Walsh, and an anonymous reviewer who offered valuable comments that significantly improved this manuscript. I also offer a special thanks to the Family of Rotiferologists, who are too numerous to mention.
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FOOTNOTES |
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1 From the Symposium Lesser-Known Protostome Taxa: Evolution, Development, and Ecology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
2 E-mail: WallaceR{at}Ripon.edu
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