Quekett]ournal ofMicroscopy, 1999,38,351- 356 351
A simple generic key to the Bdelloid rotifers
PAUL N. TURNER
Summary comparisons or genetic tests, since cross-breeding or inbreeding Rotifers of the Order Bdelloidea occupy a vast number of does not occur and cannot be natural habitatS, from ice to soil, lichens to mosses. fresh· induced. water interstitial to salrwater sands, from the tropics to the The proper identification of bdelloids requires Antarctic. Beca use of their apparently cosmopolitan that they be viewed in-vivo, which in turn requires presence, an understanding of their taxonomy is critical, special care and handling of the animals and the especially since more and more ecologists are confronted medium. Bdelloids are particularly sensitive with the need tO identify them in sampling regimes. to changes in temperature, Since descriptions such as 'rotifer sp.' or 'bdelloid sp.' light, oxygen content, and are becoming more and more unacceptable in a modern vibrations, so these factors must be controlled species list, this paper presents a relatively simple numeri· to be successful. cal key that will allow non-expens tO identify most The customary use of a high-intensity light common bdelloid rotifers to genu s. Although the Order source for microscopic examination may need to is in much need of revision at species level, the current be altered while viewing bdelloids, since the heat generic names and criteria will probably persist through generated by the light source may provoke any such revision, and thus generic-level identifications animal contraction. Likewise, produced with this key will likely be accurate in the physical vibrations future as well. in the water, on slide or watch-glass, created by focusing or by moving the mechanical stage, may induce contraction. If the animal stays con Introduction tracted for more than a few minutes, it is not likely to recover for some time. If this occurs, AccuRATE identification of Bdelloid rotifers can the viewer may be forced to wait be very difficult. Literature on rotifer taxonomy for the rotifer tO recover from the agitation, or seek seldom discusses details of the Bdelloids in another example for identification. common terms. Works that deal with the taxo· nomy of the Order in any detail are usually large, technical, and aimed at specialists. As a Background result, there are very few references of note A short history of the research, and a partial occupying the 'middle' ground between the listing of references available, amateur and specialist. begins with the many works of Murray (1902- 1913) and Bryce When presented with the identification, non (1892- 1929). They combine to assume the most specia lists t urn to the existing taxonomic refer significant baseline information used for the ences, but this difficult chore is compounded in later works on taxonomy and ecology of three ways. (1) the subtleties of acceptable specific Remane (1 932/33) and Voigt (1957). Subsequent features, (2) concurrent questions about what is a works by Bartos (1951 ) in English, and Donner true species in a completely parthenogenetic (1965) in German, are the most recent and most group of animals, and (3) the difficulties of detailed compilations of significance. Additional bdelloid rotifer handling. Suitable identifications efforts include Koste & Shiel (1986) discussing are also hindered by the extreme amount of Australian bdelloids as a part of a series on time usually required of the investigator in the Australian rotifers, and the six works of H aigh attempt to wade through the subtle specific (1963- 1971) that discuss New Zealand bdelloids. elements for good identifications. As a result, These later works are among the last compre "b delloid sp." too often shows up on microfauna hensively to examine the taxonomy, ecology and lists. systematics of the Order. Non-taxonomic The entire Order Bdelloidea (bdelloids) con research in the o rder is described by Bateman & sists only of female rotifers. There are no Davis (1980), Ricci (1987), Zullini & Ricci (1980), known males. In one sense this simplifies the and others. chore of identification, since there is only one The current state of understanding is au_gmen gender for which to accumulate identification ted by virtual works such as the Aydin Orstan elements. Without males, however, acceptable bdelloid web page a~ http://members.aol.com/ species identifications must rest on phenotypic bdelloidl/deloid.htm. Orstan discusses the entire 352 PAUL N. TURNER
group with very useful diagnostic keys, photos, treatment techniques. Donner (1965) is the drawings and ecological data. preferred, and possibly the most authoritative work on bdelloid rotifers, but published only in Discussion German. Use of other keys such as that by Bdelloid rotifers can be found in almost any TABLE 1 temporary or permanent wet environment. Generic Ide Many are considered aquatic, flourishing in the ntification Elements benthos or littoral of ponds and streams, while 1. Rostrum imperfectly developed others occupy terrestrial habitats such as moist 2. Rostrum non-retractile soil, mosses, leaf litter and lichen s. These rotifers 3. Wheel organ (ciliated field) prone and flat are notable for their ability to resist severe 4. Wheel organ ring, with dorsal and ventral breaks environmental changes to their habitat. The pro 5. Upper (dorsal) lip undivided cess and morphology of their ability to resist 6. Upper (dorsal) lip bilobed, or divided dehydration (anhydrobiosis) is documented in 7. Pedicels rudimentary, or absent Jacobs (1909), Rahm (1926), Ricci (1987) and 8. Pedicels well developed Umezawa (1958) to mention a few. Only a rela 9. T rochal disc inset, between 2 horn-like processe.s 10. Trochal tively small number of specific bdelloid r otifers disc between hoodlike expansion of upper lip have been actually documented performing 11. Throat anhydrobiosis, (Philodina distinct roseola, Adineta vaga, 12. Gullet absent Macrotrachela musculosa, Mniobia magna, Macro 13. Rami protrusile trachela quadricornifora, Habrotrocha constricta, 14. Lumen wide Philodina acuticornis odiosa, Mniobia russeola) 14a. Lumen absent, where food pellets 611 body cavity under special, slow drying conditions (Gilbert, 15. Lumen narrow 1974), yet the process is logically extrapolated 16. Food in pellets (do not mistake oil droplets for for the rest of t he Order by their reappearance food) in the moss, lichen and soil habitats in which 17. Food NOT in pellets they often occur. 18. Abdominal transverse cuticle folds correspond to body segments Non-bdelloid species (those of the other major 19. Abdominal transverse cuticle folds numerous, class of Rotifera, Eurotatoria (Monogononta)) NOT corresponding with body segments also sometimes suddenly reappear in open perma 20. Foot long, slender nent or temporary waters after a long stretch of 21. Foot short, stout dryness. The mechanism responsible for their 22. Foot ending in sucker-like plate, disc or discs presence can be attributed to an equally significant 23. Foot glands in longitudinal series survival phenomenon of laying resting or 'resis 24. Foot glands in transverse series 25. Foot shorter than pre-intestinal tant' eggs, prior to, or during environmental part 26. Toes 2 stressful conditions such as the evaporation of 27. Toes 3 their water habitat. This phenomenon is thought 28. Toes 4 to be an extension of their ability to reproduce 29. Spurs 1 parthenogenetically, which includes episodes of 30. Spurs 2 males appearing and joining with females to 31. Spurs long produce 'resting' eggs and a new generation of 32. Spurs short parthenogenetic females. 33. Spurs modified or absent 34. Cuticle coarse, leathery, bumps, spines, There are too few rotifer taxon plates or omic references knobs properly to support bdelloid rotifer identifi 35. Viviparous (able to see young forming inside cations for the non-specialist. Ongoing research mother) by interested ecologists, environmentalists and 36. Oviparous other biological workers has suffered from a 37. Commensal lack of suitable references to assist even the 38. Limnetic (free-swimming) simplest of bdelloid rotifer identifications. 39. Anhydrobiotic (found in moss) Works such as Pennak (1978) offer a modicum 40. Eyes generally absent of help, but the arrangement of key elements 41. Eyes cervical or in neck, rarely absent 42. Eyes in rostrum can sometimes be confusing, and some primary or rarely absent 43. T rophi aberrant elements of identification are not visible without 44. Sometimes in 'bottle' secretion shell the application of suitable and often difficult A simple generic key to the bdelloid rotifers 353
Koste & Shiel (1986) (for Australian fauna), Dorsey of Philadelphia, Pennsylvania, during although adequate for genera, can be misleading their cooperation in rotifer research. Modifica for species if used for other parts of the world, tions to the Myers key were made by Alben E. since rotifers in general are now being acknowl Turner Ill, in his unpublished aborted attempt edged to be endemic to a larger extent than to revise the Order. Noticeable elements of previously thought (Ricci, 1987). Relying on important characters are taken from Bryce experts for bdelloid rotifer identifications can (1910), Bartos (1951) and Donner (1965). also be difficult, since such people are all too few. The Tables are arranged into Generic Identifi cation Elements (Table 1), and the Numeric Key The Key of genera based on Table 1. A simplistic This paper is designed to be a non-specialist diagram of important bdelloid identification elements identification key, aimed at the individual can be seen in Figures 1-6. The most researcher in need of an identification tool for 'common' bdelloid rotifers that bdelloids. investigators are likely to encounter are worm like animals that possess two distinct anterior Tables 1 & 2 will allow a worker to have a ciliated wheel-bodies or discs (Figures 1 & 2). reasonable chance of getting a bdelloid identifi The first wheel-body sits on short or long, usually cation down to genus, but not to species. It does separated pedicels, accented by cilia around the not follow the traditional 'key' structure, but it top (sometimes with a mid-placed sensory hair) does follow a key-code format that prove will and is called the trochus. (Some diagnostic charac useful to those who attempt tO get past the all teristics of the trochus include breadth and too pervasive 'bdelloid sp.' they find themselves distance between pedicels, relative thickness, obligated to report in the literature. height above secondary wreath (cingulum) and This key (the combination of Tables 1 and 2) proportion in breadth to head.) The second has been patterned after one used by Frank wheel-body rests on the base or lower lip of the J. Myers, subsequently shared with Louis pedicel, and is called the cingulum. These can
TABLE 2 A Numeric Key of genera based on Generic Identification Elements
GENUS Generic ID Elements Additional Characteristics
Adineta 2 3 20 27 33 large ventral ciliated field Bradyscela~ 2 3 21 27 33 papillae for toes Ceratotrocha~ s 7 -9 14 16 36 40 Didymodact:ylos * 12 13- IS 17 26 Zelinkiella"· 1s 17 22 24 3S 37 commensal on sea cucumbers Dissotrocha 6 11 1s 17 18 28 31 34 3S usually cuticular spines, sometimes plates Embata 6 1S 17 28 31 36 37/38 corona wide, usually free swimming or commensal Habrotrocha S 8 14a 16 27 36 44 usually on mosses Macrotrachela S/6 }f172S27 ~ 36 40 Otostephanos -4 s 8 14 -16 36 40 Mniobia 1s 17 22 23 2S 36 40 sucker-like disc vice toes Philodina 6 11 1- s 17 28 32 36 41 Philodinavus* 2 28 43 Pleuretra 6 11 1S 17 19 28 34 36 40 armor-like dorsal cuticle Rotaria 6 1S 17 -27 3S -42 Scephanotrocha s 7 10 14 16 36 40 - - Abrochtha* 12 13 1S 17 28 Anomopus'' IS 17 20 22 23 foot ends in discs Henoceros 28 29 43 corona absent, large, fat toes
* = rare or monotypic. Underlined numbers (_) are primary elementS. 354 P AUL N. T URNER
B J D c
1 4 ----
-r---E
G
H H
3b G f-- A • )::~~~ .•. • 5 • • • •• • I ••.. ;. .. .. 2b ...... _~---- . \~;~ .. ~ '1'"~; ' o ....!;:,,:.• I • A • • • • •• I •• ' ' "' ,l ...... •.••• . 6 •. . .*. .0 . , I I• o I .• • t ; • • . 3a LJ --t-:·~· I I • ",. •' • .., .. -,,If ...... ,.•',F ·~ B - • ..;I I • '. L/E K ' ' '!..-'-"' · --:.-:~..-:l':'t.-.. ~) '"' ·., _) •. '. ..
KEv: A: Rostrum; B: Wheel Organ; C: Cingulum; D: Pedicel; E: Foot; F: Toe; G: Spur, H: Mouth Area; I: Antenna; J: Lip and K: Trophi.
Fro. 1. Dorsal view of adult female 'generic' bdelloid rotifer head (not contracted). Fro. 2a. Ventral view of adult female 'generic' bdelloid rotifer head (not contracted). Fro. 2b. Left lateral view of adult female 'generic' bdelloid rotifer anterior half (not contracted). Fro. 3a. Ventral view of adult female 'generic' bdelloid rorifer anterior half (contracted). Fro. 3b. Dorsal view of adult female 'generic' bdelloid rotifer (contracted). FIG. 4. Dorsal view of adult female 'generic' bdelloid rotifer foot. FIG. 5. Lateral view of adult female 'generic' bdelloid rotifer foot. FIG. 6. Dorsal view of generic rami bdelloid trophi. A simple generic key to the bdelloid rotifers 355
generally be seen when the animal is observed Acknowledgements feeding or swimming and are collectively referred Many tO as the corona. Ventrally, the animals mouth thanks to Claudia Ricci for her comments and catches food swirled into it by the corona's ciliary suggestions. action. (The animal's treatment of food, ie PAUL N TURNER formation into pellets or not, can be diagnostic.) 1003 Suuers Rim San Amonio, Texas, 78258 The presence, absence and location of eyes, USA presence of a ventral and/or dorsal lip, shape and size of dorsal rostrum (proboscis) and dorsal antenna compose many of the key elements Literature Cited to the anterior anatomy of the bdelloid rotifer. E. BARTOS [1951] - The Czechoslovak Posterior elements consist of false Rotatoria of toes called the Order Bdelloidea, Vestmk Ceskos/O'Uenski spurs, foot segments and true toes, which are all Zoologicki Spolecnosti v Praze, 5, 241 - 498. diagnosed by shape, size and number (Figures L. E. BATEMAN & C. C. DAVIS [1980] - The Rotifera of 3b, 4 & 5). Their bodies are pseudosegmented Hummock-Hollow Formations in a Poor and extremely telescopic, which can conceal the (Mesotrophic) Fen in Newfoundland. lnter nature of their cuticle, which by itself can be diag nationale Revue der Gesamten Hydrobiologie, 65, 127- 153. nostic (look and feel, number of longitudinal or D. BRYCE [1917 transverse folds, pseudo-armature such as spines, ] - Notes on the collection of Bdelloid and other Rotifera, journal bumps, warts, hooks of the Quekett etc., and secreted, bottle Microscopical Club, ii 13, 205- 230. like shell). D. BRYCE [1922] - On some Rotifera from Spitsbergen. Both the presence of two trochal discs (absent The Oxford University Expedition to Spits in Adineta, Henoceros, Philodinavus, and Bradys· bergen, 1921,journal ofthe Quekett Microscopical Club, 4, 305-332. cela) and their leech-like creeping motion are D. BRYCE mostly key to initially identifying the observed [1915] - On Five New Species of the Genus Habrotrocha, Journal animal as a bdelloid rotifer of the Quekett . The jaws (trophi) Microscopical Clt
Diogononta), Australian journal of Marine and ) . MuRRAY [ 1908] - Arctic rotifers collected by Dr. Freshwater Research, 37, 765- 792. William S. Bruce, Proceedings of the Royal Physi· ). MURRAY [1902] - Some Scottish Rotifers, with descrip ea/ Society ofEdinbur gh. 17, 121-127. tions of new species, Annals of Scottish Natural A. ORSTAN [1998] - An Introduction to Bdelloid Rotifers. History, 54, 162- 167. http://members.aol.com/bdelloid1/deloid.htm ). MURRAY [1911] - Bdelloid Rotifera of South Africa, R. W . PENNAK [1978]- Fresh Water invertebrates ofthe Annals ofthe Transvaal Museum , 3, 1- 19. United States. 2nd edition. Wiley, New York, 1- 802. ). MURAY [1911 ] - Australian Rotifera: Collected by the Shackleton Antarctic Expedition, 1909, P. G. RAHM [1926] - Die Trochenstarre (Anabiose) journal of the Royal Microscopical Society. April, der Moostierwelt Biologisches Zentralblatt, 46, 164-174. 452- 477. ). MURRAY [1911] - Canadian Rotifera: Collected by A. REMANE [1932/33] - Rotatorien. in Bronn, H. G. ed, the Shackleton Antarctic Expedition, 1909, Klassen und Ordnungen des Tierreichs, vol. 4, journal of the Royal Microscopical Society. C. F. Winter, Leipzig, 1- 575. June, 285- 297. C. RtCCI [1987] - Ecology of bdelloids: how to be ). MuRRAY [1911] - Rotifera of some Pacific Islands: successful. Hydrobiologia, 147, 117-127. Collected by the Shackleton Antarctic Expedi C. RICCI, L. VAGHI, & M. MANZINI (1987)- Dessication tion, 1909, journal of the Royal Microscopical of Rotifers (Macrotrachela quadricornifera): Society. August, 429- 435. survival and reproduction. Ecology, 68, 1488-1494. ) . MURRAY [1911] - XVU. Rotifera of New Zealand: S. UMEZAWA [1958] - On the desiccation death of the Collected by the Shackleton Antarctic Expedi rotifer, Philodina roseola. Research Reports of tion, 1907- 9, journal of the Royal Microscopical the Kochi University, 7, 1- 15. Society. October, 573- 587. M. VOtGT [1957] - Rotatoria. Die Radeniere Mitteleuco ). MURRAY [1911] - XVIII. South African Rotifera: pas Gebriinder Bometraeger, Berlin. 2 vols. Collected by the Shackleton Antarctic Expedi A. ZULLINI & C. RICCI (1980) - Bdelloid rotifers and tion, 1907, journal of the Royal Microscopica/ nematodes in a small Italian stream. Freshwater Society. October, 584-587. Biology, 10, 67-72.