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Protistology an International Journal Vol Protistology An International Journal Vol. 2, Number 4, 2002 __________________________________________________________________________________________ CONTENTS Igor V. Dovgal Evolution, phylogeny and classification of Suctorea (Ciliophora) Introduction 194 Chapter 1. The origin of suctorian ciliates and the taxonomic position of the group 198 Chapter 2. Some regularities in the evolution of suctorea 203 Chapter 3. The taxonomy of some problematic suctorian genera and species 210 Chapter 4. The phylogeny of Suctorea 224 Chapter 5. Principles of taxonomy and new classification of Suctorea 238 References 264 INSTRUCTIONS TO AUTHORS 271 Protistology 2 (4), 194–270 (2002) Protistology Evolution, phylogeny and classification of Suctorea (Ciliophora) Igor V. Dovgal Schmalhausen Institute of Zoology NAS of Ukraine, Kiev, Ukraine Summary The monograph is concerned with suctorian ciliates. Using the materials collected and generalizing all literary data available, the author has proposed original hypotheses of suctorians’ origin and the main regularities of the evolution of the taxa. A new scheme of phylogeny of Suctorea has also been elaborated. Based on this research a new system of the class Suctorea, including 4 subclasses, 15 orders, 2 suborders, 41 families and 124 genera, has been proposed. Key words: Suctorea, evolution, phylogeny, classification Introduction species are planktonic. Typically they are freshwater This monograph is concerned with suctorian forms but marine species (the genus Marinecta ciliates. This group is one of the most speciesrich (531 Jankowski, 1978) have also been recorded. It seems according to our data) groups among Ciliophora likely that all representatives of this ecological group Doflein, 1901. Suctorian species constitute about 7% are secondaryly planktonic. of ciliate species that have been described to date. Morphology. Suctorian ciliates are largely sessile Habitats. Suctorians can be found in all types of forms. The adult stage (trophont) is usually the stalked water bodies on a wide diversity of hosts and substrates. zooid (Fig. 1). The unstalked flattened (Fig. 2) or The majority of these ciliates are commensals of various ramified forms are less common. The presence of one water invertebrates or vertebrates (fishes or turtles). or more tentacles, as a rule with a distal extention (knob) Suctorian ciliates also inhabit the intestine of horses, is most characteristic of the group. rhinoceroses, guinea pigs and elephants (Timoshenko, The ciliature is lacking in trophonts of suctorians 1996; Van Hoven et al., 1998, and others). (except the commensals of guinea pigs). Only in the There are both ectoparasitic and endoparasitic ventral zone near the contractile vacuole canal a small species among suctorians. These ciliates often parasitize field of barren kinetosomes with reduced ectoplasmic on other ciliates including suctorians. The parasites of fibrils may occur (Seravin and Gerassimova, 1978). multicellular organisms such as rotifers, molluscs, The body of suctorian trophonts characteristically sabellid polychaetes, turbellarians are also known. ranges in size from 100 µm to 200 µm but certain Several podophryid and trichophryid suctorian ophryodendrid suctorians may be as large as 800 µm, © 2002 by Russia, Protistology Protistology · 195 while Dendrosoma radians Ehrenberg, 1838 reaches 2000 µm (Dovgal, 1996) or even 5000 µm (Batisse, 1994). The body shape of suctorian trophonts is widely diversified, which has been associated with sessile mode of life, substrate diversity, environment factors and lack of cilia (Batisse, 1994), with the substitution of the cytostome (a characteristic centre responsible for ciliate shape) by numerous tentacles (Dovgal, 1996). Interestingly, coloniality is presumably not characteristic of suctorian ciliates. Exoskeleton is present as different stalks and loricas. Besides lorica, completely covering the ciliate body, semilorica or basotheca, covering only the lower part of the body is often observed. The stylotheca (thecostyle) represents type of loricas. The organisms with stylotheca adhere to the substrate by means of their stalklike protuberance. The mucous lorica forming at the expense of the glycocalyx development is not uncommon in Suctorea as well. There is invariably one macronucleus in suctorians. The macronucleus varies in shape from spherical or oval (in small species) to ribbonlike or branched (in large species). The micronuclei are generally numerous in suctorian ciliates and unevenly distributed around the macronucleus or (rarely) within the depressions in the latter. There are contractile vacuoles in suctorians of all Fig. 1. Discophrya elongata (Claparede et Lachmann, ecological groups: freshwater, marine and parasitic. The 1859) from the leg of water bug Ranatra linearis number of contractile vacuoles can vary in accordance (Linnaeus, 1758). Scanning electron microscopy with suctorian species, age and size. For example, there (х1200). Abbreviations: tn – tentacle; z – zooid; st – are mainly one or two vacuoles in exogemmin and stalk. endogemmin suctorians, whereas numerous vacuoles Fig. 2. Dendrocometes paradoxus (Stein, 1851) from the gill of gammarid amphipod Gammarus lacustris Sars, 1863. Scanning electron microscopy (х860). 196 · Igor V. Dovgal (up to several tens in Discophrya ochthebii Matthes, taxonomic rank of the group, numbers of subordinate 1954) may occur in inversogemmin suctorians. taxa, etc. (Jankowski, 1978, 1980, 1981; Matthes et al., Life cycle and development. Just like other sessile 1988; Batisse, 1994; Dovgal, 1996). ciliates suctorians as a rule reproduce by different modes There are two main approaches to the derivation of budding. Their life cycle consists of a freeswimming of the Suctorea system. larval stage (swarmer) that (except vermigemmins) D. Matthes and his followers believe that the possesses locomotor ciliature. The morphology of classification should be elaborated on the basis of non suctorian swarmers is less diverse than that of trophonts. adaptive characters. Naturally, the adoption of such a Still attempts at their classification have been made limited group of characters hampers the development (Guilcher, 1948a, 1951; Batisse, 1994). of a rational classification. Furthermore, the problem The reproduction by monotomy is retained in of nonadaptive nature of morphological characters is parapodophrians, parasitic sphaerophryans, ambiguous. This seems to be the reason why D. Matthes phalacrocleptid suctorians as well as in intestine did not necessarily use the principles proclaimed in inhabitants. Certain parasitic species (for example, regard to suctorians. In particular, the shape of Sphaerophrya parameciorum Maupas, 1881) reproduce macronucleus was not used in suctorian taxonomy by both monotomy and budding (Jankowski, 1963). (Matthes et al., 1988). In some tokophryid suctorians trophotomy or Another approach to construction of the Suctorea reactive budding may occur under adverse conditions. classification was stated by A.V. Jankowski (1978, 1980, In the course of trophotomy the entire trophont 1981). This author has proceeded from the assumption generates locomotor ciliature and then breaks away that if the organisms differ from the characteristics of from the stalk. However, it is strictly speaking not their group only by one sufficient character they must reproduction, as it does not result in an increase in the be classified in separate taxon. Only presence or absence number of individuals. of a character may be used as a basic guideline for The swarmer attaches to a substrate suitable for classification, and not the degree of character settlement. Shortly after settling, it undergoes distinction. metamorphosis involving resorption of the ciliature and Several other versions of the Suctorea classification development of the stalk, lorica (if present) and (Corliss, 1979; Dovgal, 1996, etc.) might be considered tentacles from the tentacle anlages (Bardele, 1970; as compromise settlements. However, the recent Dovgal, 2002). classification of A. Batisse (1994) is worth special The modes of suctorian reproduction hold much consideration. The author has proposed to discriminate systematic significance and will be discussed below. three suctorian orders that differ by the mode of Feeding. Suctorian ciliates capture and devour their budding. For representatives of the order Podophryida prey by tentacles. No less that 10 hypotheses of the Jankowski, 1973 exogemmy without any invaginations functioning of suctorian tentacles can be enumerated (“heteromorphic division”) is characteristic. The order (Hertwig, 1875; Plate, 1886; Eismond, 1891; Collin, Exotropida Batisse, 1994 includes the forms with 1912; Penard, 1920a; Kahl, 1931; Kormos, 1938a; exogemmy that starts with invagination of the cortex Kitching, 1952; Hull, 1961; Bardele, 1972, etc.). A full (mainly ephelotins and ophryodendrids). Finally, consideration of most of them is contained in M. internal budding of the representatives of Entotropida Canella’s (1957) monograph, many of the hypotheses Batisse, 1994 begins with invagination. As a result, the being mainly of historical interest. suctorians with both ciliary and nonciliated swarmers Suctorian ciliates exhibite a certain selectivity as fall into Exotropida and those with internal and external regards food objects (Canella, 1957). Freeswimming budding (parapodophryans, thecacinetins, etc.), into ciliates are the basic prey of suctorians. Capture of Entotpopida. This classification constitutes a radical
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