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Glossary
- Acanthocephala:
-
Parasitic worms characterized by a retractable proboscis with spines and hooks that it uses to be securely attached at their hosts. They have complex life cycle and are considered a sister taxon of Rotifera.
- Amictic:
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Adjective that indicates the absence of mixing or exchange. In rotifers, it indicates females with asexual reproduction or a diploid egg which have not been fertilized.
- Bdelloids:
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Class of rotifers with trophi ramate and wormlike body. Approximately 360 species with obligate parthenogenetic reproduction and paired ovaries. They live on surfaces (plants or stones) or on the sediments.
- Biomarker:
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Measurements of alterations in biological components, structures, behaviors, or biochemical, physiological, and genetic processes, resulting from sublethal exposure to xenobiotics in an organism.
- Carbamate:
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Organic compounds derived from carbamic acid, widely used as insecticides. Their inhibition of acetylcholinesterase is relatively reversible. They have a low environmental persistence.
- Corona:
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Ciliated anterior region used in locomotion and food gathering.
- Dimorphism:
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Differences or changes in the external appearance of males and females of the same specie (size, shape, color, behavior).
- Diploid:
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Organism having two sets of chromosomes, usually one from each parent
- Endpoint:
-
It is a response which is measured in a living organism during an ecotoxicological test, and it registers a potential adverse effect on individual and population levels.
- Fungicide:
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Chemical compounds used to kill or inhibit fungi or fungal spores.
- Haploid:
-
Organism having only one complete set of chromosomes.
- Herbicide:
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Substance used to eliminate unwanted plants.
- Illoricate:
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Organisms with a thin and flexible integument (e.g., families Conochilidae, Notommatidae, Proalidae).
- Loricate:
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Organisms in which extensive regions of the integument are thicken and rigid (e.g., families Brachionidae and Lecanidae).
- Mastax:
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Pharynx of rotifers with powerful muscular wall that contains tiny, calcified, jawlike structures called trophi.
- Mictic:
-
Adjective that indicates mixing or exchange. In rotifers, it indicates a haploid egg produced by sexual reproduction. Eggs with fertilization produce cysts and amictic females. Unfertilized eggs produce males.
- Monogonont:
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Class of rotifers found mostly in freshwater, but also in soil and marine environments. 1,600 species with sexual or asexual reproduction, a single ovary, and trophi with many forms, except fulcrate or ramate. There are species from free-swimming to sessile.
- NB:
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Sources of these definitions are from Dodson (2005), Wallace et al. (2006), and Manahan (2003) (see References section of this entry).
- Organochlorine:
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Organic compound containing at least one covalently bonded chlorine atom. The organochlorine insecticides enjoyed wide use in agriculture insect control and malaria control programs. Their acute toxicity is moderate, but chronic exposure may be associated with biomagnification and adverse health effects, particularly in the reproductive system.
- Organophosphate:
-
Esters of phosphoric acid. Type of synthesized insecticides with low persistence and bioaccumulation, but high neurotoxicity. These compounds inhibit acetylcholinesterase which producing accumulation of acetylcholine in cholinergic synapsis. Accumulation of acetylcholine results in continued stimulation of acetylcholine receptors, which can cause numerous effects related to excessive nerve response.
- Parthenogenesis:
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Type of asexual reproduction where one or a few diploid eggs are produced and are genetically identical to the mother. Thus, the offspring of a single adult constitute a genetic clone.
- Pesticide:
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Substance or mixture of substances intended for preventing, destroying, repelling, or mitigating any pest.
- Pseudocoelomate:
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Organisms possessing a “pseudocoel” (false cavity) which is a fully functional body cavity (it contains muscles, nerves, and digestive, reproductive, and protonephridial organs). A body cavity is any fluid-filled space in a multicellular organism.
- Trophi:
-
Hard parts (jaws) of mastax that articulate in a specific spatial arrangement. It has taxonomic importance for characterizing families, genera, and often species. There are nine types of trophi based on size and shape of functional units (uncus, ramus, manubrium, fulcrum, alula).
Definition
Rotifers (Rotifera), commonly named wheel animals, refer to a taxonomic group of small aquatic invertebrates employed in aquatic ecotoxicology to measure adverse effects of chemical contaminants and complex environmental samples under both laboratory and field conditions.
Marked contributions to the field of ecotoxicology provided by studies conducted with rotifers are reported herein. Emphasis is placed on the acute sensitivity of rotifers to three groups of toxicants: metals, organic compounds, and pesticides. The main characteristics of Rotifera, species used for ecotoxicological studies, endpoints, and various other aspects, are also featured. Research prospects for rotifers in ecotoxicology will profit from studies seeking to better understand the relationship between phylogenic distance and species sensitivity to toxicants. Appraising more species of rotifers to determine their sensitivity to a wider variety of toxicants is also to be encouraged. Lastly, recent breakthroughs in environmental genomics suggest that this field of expertise could gain when applied to environmental investigations undertaken with rotifers.
Overview
The phylum Rotifera refers to a taxonomic group of aquatic pseudocoelomate invertebrates characterized by the presence of a ciliate corona and a strong muscular mandible called mastax, formed by a jawlike structure called trophi, and a body wall that might be thickened, in the case of loricate taxa, or not, in the case of illoricates (Wallace et al. 2006). Figure 1 shows Lecane quadridentata, a loricate rotifer, and Fig. 2 shows Asplanchna brightwellii, an illoricate rotifer.
Taxonomy and Systematics
Although they were considered a phylum for many years (Wallace et al. 2006), the current view is that rotifers do not represent a monophyletic taxon and that they belong to the Syndermata, a phylum that includes the typical rotifers (Monogononta, Bdelloidea, and Seisonaceae), and the acanthocephalans (Min and Park 2009). Rotifers of the Monogononta (by far the most diverse class) reproduce mostly through parthenogenesis by amictic females when the environmental conditions are stable. However, several stimuli such as high population density, chemical compounds, salinity, changes in temperature, and quality or quantity of food can induce sexual reproduction with a remarkable dimorphism between females and males in many species (Fig. 3). Sexual reproduction is carried out by mictic (diploid) females that produce haploid eggs. The unfertilized haploid eggs produce males that have short life spans, which fertilize the haploid eggs in the interior of the mictic females producing diploid resting eggs (or cysts). Following a period of latency, and when environmental conditions become favorable, the cysts give origin to amictic females that initiate the parthenogenetic cycle again (Dodson 2005; Wallace et al. 2006). Rotifers of the class Bdelloidea are completely asexual, and no male has ever been found in this class. The class Seisonaceae is currently composed of two parasitic species of obligate sexual reproduction (Dodson 2005).
Rotifers Used in Ecotoxicology
Rotifers have many characteristics that favor their use as test models for ecotoxicological studies: ease of culture, exponential growth, small size, and sensitivity (Dahms et al. 2011). Many species have been cultured. The importance and relevance of rotifers as members of the zooplankton, and as primary and secondary consumers in many aquatic trophic webs, is well documented (Wallace et al. 2006). In some species of the genus Brachionus, production of cysts (that can be stored dry at room temperature) is possible. The ability to produce cysts has allowed the development of toxicity kits, called Rotoxkits, employed for acute/chronic marine and freshwater toxicity testing (http://www.microbiotests.be). Cyst production is an outstanding characteristic that has enabled the development of several toxicity protocols using rotifers. In fact, toxicological protocols using eggs obtained by parthenogenesis have been reported for the production of clonal cultures of rotifers. However, the scale of egg production must be optimized to obtain sufficient amounts of DNA material for the undertaking of molecular toxicology studies.
Unfortunately, the database of toxicants investigated with rotifer species is small in comparison with data for other model organisms like Daphnia magna, Drosophila melanogaster, or vertebrate species (US Environmental Protection Agency 1997), and the taxonomic status of the two rotifer species most used in ecotoxicology (Brachionus calyciflorus and Brachionus plicatilis: sees Table 1–3) is doubtful as they belong to species complexes, in contrast with cladocerans where species status is better established.
Protocols for acute testing using rotifers are straightforward and consist in the hatching of neonates from cysts 18 or 28 h before start of test (Snell and Janssen 1995) or from parthenogenetic eggs 24 h before start of test (Pérez-Legaspi and Rico-Martínez 2001). Neonates are then transferred to synthetic fresh- or saltwater medium with the correspondent toxicant or control concentration and incubated at 25 °C for 24 or 48 h typically. After the incubation period, the number of dead rotifers is counted, and the LC50 values are calculated (in general using probit analysis of commercial or freely available software).
Modern toxicity studies using rotifers as model organisms started as early as 1964 (Cairns et al. 1978). However, a significant increase in contributions using rotifers for ecotoxicological studies started in the 1990s (Snell and Janssen 1995). Only three genera and seven species of rotifers were reported by Snell and Janssen (1995) for single-species acute or sublethal toxicity testing: five monogononts (Brachionus calyciflorus, Brachionus patulus, B. plicatilis, Brachionus rubens, Dicranophorus forcipatus) and two bdelloids (Philodina acuticornis and Philodina roseola). Globally, nine other genera comprising 28 species now comprise additional taxa available to produce measurement endpoints (e.g., LC50 or EC50 values) with well-defined protocols. These additional taxa include the following: Adineta vaga (Orstan 1992); Anuraeopsis fissa (Sarma et al. 2007); Asplanchna brightwellii (Enesco et al. 1989); Asplanchna girodi (McDaniel and Snell 1999); Asplanchna intermedia (Smith et al. 1988); Asplanchna sieboldi (Sarma et al. 1998); Brachionus angularis (Gama-Flores et al. 2004); Brachionus caudatus (Daam et al. 2010); Brachionus havanaensis (Juárez-Franco et al. 2007); B. patulus (Sarma et al. 2006), called Plationus patulus by McDaniel and Snell (1999); Brachionus macracanthus (Nandini et al. 2007); Brachionus rotundiformis (Araujo et al. 2001); Brachionus urceolaris (Hatakeyama 1986); Brachionus urceus; Euchlanis dilatata (McDaniel and Snell 1999), Euchlanis sp. (Daam et al. 2010); Filinia longiseta (Qin and Dong 2004); Keratella americana (Vancil 1976); Keratella cochlearis (Liber and Solomon 1994); Keratella quadrata (Qin and Dong 2004) Keratella tropica; Lecane closterocerca (Daam et al. 2010); Lecane luna; Lecane hamata (Pérez-Legaspi and Rico-Martínez 2001); L. quadridentata; Lepadella patella (McDaniel and Snell 1999); Philodina acuticornis odiosa (Hagen et al. 2009); and Trichocerca pusilla (McDaniel and Snell 1999). Assessment endpoints determined in rotifer toxicity studies are varied and have included the following: mortality (with exposure times of 30 min, 24 h, 48 h, or 96 h, as reported in Tables 1, 2, and 3), reproduction inhibition and behavior (see review by Snell and Janssen 1995), enzyme biomarkers (Burbank and Snell 1994; Araujo et al. 2001; Pérez-Legaspi et al. 2002; Pérez-Legaspi and Rico-Martínez 2003; Arias-Almeida and Rico-Martínez 2011), mRNA biomarkers (Cochrane et al. 1994), induction of stress proteins (Wheelock et al. 1999; Kaneko et al. 2002, 2005; Rios-Arana et al. 2005; Suga et al. 2007), and predator–prey interactions (see review by Preston 2003).
Species Sensitivity Distributions
Versteeg et al. (1999) studied species sensitivity distributions in zooplanktonic species for 11 different toxicants among metals, surfactants, and pesticides. Sensitivity distributions were derived from single-species chronic toxicity assays. In all cases, species sensitivities differed by 2–4 orders of magnitude, and the sensitivity of tested species varied considerably among toxicants. Rotifers of the genus Brachionus were among the most sensitive to dodecyl sulfate, alkylbenzene sulfonate, and copper, but least sensitive to lindane.
McDaniel and Snell (1999) assessed the sensitivity distributions among nine species of rotifers in response to cadmium and pentachlorophenol (PCP) exposure. Sensitivities differed by two orders of magnitude for both toxicants. Relative sensitivity among species varied with the toxicant as well as the measurement endpoint (24-h mortality or 30-min in vivo esterase activity). Pérez-Legaspi and Rico-Martínez (2001) compared the sensitivity of 11 different compounds (organics and metals) among three species of the genus Lecane: L. hamata, L. luna, and L. quadridentata. The highest interspecies differences in LC50 values (22-fold) were found in the sensitivity to lead.
Studies with Mesocosms and Microcosms
Although mesocosm and microcosm experiments have been performed using rotifers, the latter are often simply included as part of a zooplanktonic assemblage, and little attention is paid to effects that toxicants can have on this particular taxon. There are, however, a few studies that incorporate effects of toxicants to rotifers (Snell and Janssen 1995). In Little Rock Lake, Wisconsin, Gonzalez and Frost (1994) studied the effects of acidification on rotifer species and compared those effects to what they found in laboratory experiments conducted with individual species under different pH regimes. Under food limitation conditions in laboratory experiments, Keratella cochlearis displayed reduced survivorship and reproduction, while Keratella taurocephala was unaffected. In contrast, acidification of Little Rock Lake resulted in a decrease in food availability for both species. Furthermore, K. cochlearis declined in abundance, while K. taurocephala increased in abundance due to the reduction of invertebrate predators. Rico-Martínez et al. (1998) studied the natural assemblage of a dam in Mexico that was transferred to a microcosm and then spiked with copper sulfate. K. cochlearis, B. calyciflorus, and Platyias quadricornis were the rotifer species most resistant to copper addition, while Asplanchna priodonta, Lecane bulla, and Pompholyx sulcata were the most sensitive. Addition of copper sulfate drastically reduced zooplankton densities, and recovery of the most resistant species of cladocerans, copepods, and rotifers was only observed after more than 2 weeks. Sugiura (1992) implemented an aquatic microcosm containing a planktonic assemblage that included two rotifers (Philodina and Lepadella). He added several toxicants in the presence of polypeptone: Cu2+, 2,4,5-trichlorophenoxyacetic acid (2,4,5-T), DDT, β-isomer of 1,2,3,4,5,6-hexachlorocyclohexane (β-HCH), and lindane. With a nutrient (polypeptone) at 100–500 ppm and 2,4,5-T at 10–100 ppm, rotifer species were eliminated. No such elimination occurred with copper concentrations up to 0.4 ppm. The population densities were affected by β-HCH at 0.1–3.0 ppm and lindane at 0.01–5.0 ppm in the early stages of the succession, but the population densities became closer to those of the control as the succession advanced. Addition of DDT up to a concentration of 0.5 ppm resulted in small changes in the densities of rotifers.
Koteswari and Ramanibai (2004) investigated the effects of a tannery sewage effluent on a zooplankton assemblage microcosm. They found that the magnitude of changes in the relative abundance of diatoms and rotifers was much greater than that of green algae, cyanobacteria, copepods, and cladocerans. They also observed that the plankton community response to a toxicant can be nonlinear and that relative abundance and taxonomic composition changes occurred at high concentrations of effluent. Daam et al. (2010) conducted an 8-week microcosm experiment to study the effects of the fungicide carbendazim on a zooplankton assemblage. The genus Keratella was the most sensitive among rotifers. Other rotifer taxa (B. caudatus, B. calyciflorus, L. closterocerca, Euchlanis sp.) were shown to increase in abundance.
Dynamics of Natural Populations
Eutrophication studies conducted with rotifers in the field have been numerous since 1973. These studies found that water-enriching nutrients increased the populations of several species of the genera Asplanchna, Keratella, and Trichocerca. Moreover, Polyarthra dolichoptera became scarce due to eutrophication (Wallace et al. 2006). Adverse effects of insecticides and herbicides in rotifers were investigated in experimental ponds, where the most frequently reported response was a change in community structure from dominance by Daphnia to dominance by small zooplankters such as rotifers (Hanazato and Kasai 1995; Hanazato 2001). In Canadian ponds, Kreutzweiser et al. (2002) found that 0.70 and 1.75 mg/l of the pesticide azadirachtin produced adverse effects on rotifer communities. Effects of acidification on rotifers that change community structure have also been investigated (Havens 1992; González and Frost 1994). Monteiro et al. (1995) studied metal stress in the Sado River in Portugal. They indicated that Philodina sp., and to a lesser degree Lecane luna, tolerated high concentrations of Cu, Zn, and Cd.
Miscellaneous Studies Involving Rotifers
A limited number of studies involving rotifers have been reported on nonpoint and point source pollution: municipal solid waste pollution, lotic and lentic systems appraisal, and watershed land use. Park et al. (2005) conducted toxicity testing with Brachionus plicatilis to determine LC50 values for Korean wastewaters, reporting acute toxicity from industrial, rural, and urban wastewater (see Table 2). Sarma et al. (2003) showed that Mexico City urban wastewater affects instantaneous growth rate of Brachionus patulus. Acute 48-h lethal effect measurements generated with Lecane quadridentata on municipal, industrial, and agricultural sites around the city of Aguascalientes, Mexico, indicated that most samples tested were toxic (Santos-Medrano et al. 2007). Isidori et al. (2003) employing B. plicatilis in 24-h toxicity tests found that all samples of municipal solid waste landfills in southern Italy expressed acute toxicity.
José de Paggi and Devercelli (2010) examined the influence of watershed land use on microzooplankton around the city of Santa Fe in Argentina. Six rivers and a shallow lake located in rural and urban areas were sampled during 4 weeks. River microzooplankton abundance and rotifer species assemblages were found to be good indicators of land use. Indeed, species composition was linked to a gradient along conductivity, pH, and chlorophyll a. Brachionus spp. were associated with saline waters in rural areas and Keratella spp. (except Keratella tropica) with urban water bodies.
Bioconcentration and Structure-Activity Studies
Studies aiming to determine bioconcentration factors for chemicals and QSARs (quantitative structure-activity relationships) with rotifers are limited. Bioconcentration factors (BCF) have only been reported with three species of rotifers. BFCs were calculated under laboratory experimental conditions with Brachionus calyciflorus for selenium (Dobbs et al. 1996) and PCBs (Joaquim-Justo et al. 1995), as well as for mono-, di-, and tributyltin with Brachionus plicatilis (Hong-Wen et al. 2001). A BCF of 49,300 for lead on the predator rotifer Asplanchna brightwellii was calculated from data collected in a field study. This was the first report documenting lead biomagnification by a high trophic level organism (Rubio-Franchini and Rico-Martínez 2008). Versteeg et al. (1997) studied effects of surfactants with B. calyciflorus by conducting chronic toxicity tests. They found that N-containing amines and quaternary ammonium compounds displayed the greatest toxicity followed by nonionic compounds. Based on their data, they were able to develop a useful parametric QSAR model of prediction.
Endocrine Disruption
Monogonont rotifers are particularly designed for the study of endocrine disruption, because their life cycle sometimes alternates between sexual and asexual generations. Since the pioneering work of Snell and Carmona (1995) showing that sodium pentachlorophenol (PCP), cadmium, chlorpyrifos, and naphthol inhibit sexual reproduction in Brachionus calyciflorus, many studies have been dedicated to this topic (see review by Dahms et al. 2011). Readers interested in knowing more about endocrine disruption issues (e.g., contaminants involved and effects on varied biota) are directed to entries of this encyclopedia entitled “New Perspectives in Assessing the Effects of Endocrine-Disrupting Chemicals in Fish,” “Estrogenic Endocrine-Disrupting Chemicals,” and “Bivalves in Ecotoxicology.”
Metals and Inorganic and Organic Compounds
A wide sensitivity range for diverse metals has been reported after performing acute toxicity tests with single species of rotifers (Table 1). More toxicity data were generated with Cu, Cd, Hg, and Pb than for other metals. For lethal effects, B. calyciflorus exposure to Ag (24-h LC50 = 0.0075 mg/L) displayed the most sensitive response (Snell et al. 1991b), while B. plicatilis exposed to thallium (24-h LC50 = 100 mg/L) was markedly less sensitive (Onikura et al. 2008). For sublethal effects, Hg toxicity measured with an esterase inhibition endpoint was highest (EC50 = 1 × 10-6 mg/L) for Lecane luna (Pérez-Legaspi et al. 2002), while the least sensitive response (EC50 = 59 mg/L) resulted from Philodina acuticornis exposure to cobalt (Buikema et al. 1974). For testing with marine rotifers, salt medium concentration decreases the solubility of some metals which in turn decreases the sensitivity of organisms to such metals. This is clearly observed when 24-h LC50 values determined for Ag, Cd, and Cu with B. plicatilis, a marine rotifer typically tested at salt concentrations of 15 g/L (Snell and Persoone 1989a; Snell et al. 1991b), are compared with those of B. calyciflorus, a freshwater species essentially tested with EPA medium containing 220 mg/L of salts (US EPA 1985). In the case of Pb, however, some endpoint values for freshwater species are similar or higher than those of B. plicatilis (see Table 1).
In addition to metals, some other inorganic chemicals such as potassium, sodium, sulfate, and sodium hypochlorite have been investigated using rotifers (Snell and Janssen 1995). A list of nonpesticide organic compounds tested with rotifers is provided in Table 2. Again, salt content in the medium decreases the sensitivity of B. plicatilis to certain compounds. For instance, the B. plicatilis LC50 values for acetone, chlorodinitrobenzene, chloroform, dichlorophenoxyacetic acid, diesel fuel, hexane, phenol, and tributyltin are 1.2- (chloroform) to 5.5-fold higher (diesel fuel) than the corresponding B. calyciflorus LC50 values (Table 2).
Pesticides
Pesticides and their corresponding acute lethality responses determined using rotifer toxicity tests are shown in Table 3. Brachionus calyciflorus displayed the highest sensitivity after exposure to resmethrin (24-h LC50 = 0.04 mg/L), while the least sensitive response was generated with Brachionus plicatilis exposed to trichlorfon (24-h LC50 = 257 to 293 mg/L). In comparison, the fungicide phenol, included in Table 2, was even less toxic to Brachionus rubens (24-h LC50 = 600 mg/L).
Once again, the influence of salinity in raising LC50 values is evident. In fact, almost all B. plicatilis LC50 values are 1.3- (fenitrothion) to 32-fold higher (resmethrin) than the corresponding B. calyciflorus LC50 values for cypermethrin, fenitrothion, lindane, methyl parathion, permethrin, phenol, resmethrin, and trichlorfon. Only in three cases (chlorpyrifos, endosulfan, and pentachlorophenol) were LC50 values similar. Only in one case (3-4-dichloroaniline) was the B. plicatilis LC50 value lower than that of B. calyciflorus (see Table 3).
Conclusions and Future Research
The list of rotifer species commonly used in ecotoxicological studies has progressively grown over the years, indicating their increasing popularity and recognition by the scientific community for the role they can play toward hazard and risk assessment of chemicals and complex environmental samples. Several standardized toxicity test methods now include rotifer species of the genus Brachionus (Standard Methods 1998; American Society for Testing Materials 1998; ISO 2008). In fact, the US EPA recommended the use of Brachionus plicatilis standardized tests to British Petroleum to assess the potential toxicity of the crude oil spill in the Gulf of Mexico and of oil dispersants employed for its remediation (US EPA 2010). Commercial kits called Rotoxkits®, which make use of dormant stages of rotifers (i.e., animals hatched from cysts), are also available with freshwater and marine species for routine and research applications in water toxicity assessment.
Several issues, however, regarding future prospects and use of rotifers in ecotoxicology remain to be addressed. First, an important issue of research would involve elucidating species status using molecular techniques to analyze species complexes. That would contribute to a reliable toxicity database where the sensitivity of each species is correctly assigned, thereby avoiding possible confusion created with sibling and/or cryptic species. Preliminary studies with Brachionus plicatilis suggest that there are at least 13 different taxa of this species complex (Suatoni et al. 2006). Second, the number of contaminants thus far appraised with rotifer species to determine their acute (sub)lethal toxicity remains limited, and efforts thus far have focused on conducting such tests within the genus Brachionus. As a result, information on the sensitivity of endemic species and those of restricted distribution is lacking. There is unquestionably a need to expand the database and the number of species used. Third, field studies, microcosm/mesocosm experiments conducted with existing and emerging contaminants, as well as wastewater toxicity assessment using rotifers are still quite limited. Increased knowledge concerning effects on ecosystems would clearly result from such endeavors. Lastly, additional gains for ecotoxicology can also be made by searching for new exposure and effect biomarkers in rotifers and by applying genomic techniques to identify up- and downregulated genes crucial for environmental diagnostics. This is an arena still very much in its infancy as far as the Rotifera are concerned (Dahms et al. 2011).
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Acknowledgments
Sincere thanks to Dr. Robert L. Wallace of Ripon College, Wisconsin, two anonymous reviewers, and the book editors for their critical review of this contribution.
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Rico-Martínez, R., Pérez-Legaspi, I.A., Arias-Almeida, J.C., Santos-Medrano, G.E. (2013). Rotifers in Ecotoxicology. In: Férard, JF., Blaise, C. (eds) Encyclopedia of Aquatic Ecotoxicology. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-5704-2_89
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