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2000 ISSN 0065-1583 Polish Academy of Sciences Nencki Institute of Experimental Biology and Polish Society of Cell Biology NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY VOLUME 39 NUMBER 2 WARSAWhttp://rcin.org.pl, POLAND 2000 ISSN 0065-1583 Polish Academy of Sciences Nencki Institute of Experimental Biology and Polish Society of Cell Biology ACTA PROTOZOOLOGICA International Journal on Protistology Editor in Chief Jerzy SIKORA Editors Hanna FABCZAK and Anna WASIK Managing Editor Małgorzata WORONOWICZ-RYMASZEWSKA Editorial Board Andre ADOUTTE, Paris J. I. Ronny LARSSON, Lund Christian F. B ARDELE, Tübingen John J. LEE, New York Magdolna Cs. BERECZKY, Göd Jiri LOM, Ćeske Budejovice Jean COHEN, Gif-Sur-Yvette Pierangelo LUPORINI, Camerino John O. CORLISS, Albuquerque Hans MACHEMER, Bochum Gyorgy CSABA, Budapest Jean-Pierre MIGNOT, Aubiere Isabelle DESPORTES-LIVAGE, Paris Yutaka NAITOH, Tsukuba Tom FENCHEL, Helsing0r Jytte R. NILSSON, Copenhagen Wilhelm FOISSNER, Salsburg Eduardo ORIAS, Santa Barbara Vassil GOLEMANSKY, Sofia Dimitrii V. OSSIPOV, St. Petersburg Andrzej GRĘBECKI, Warszawa, Vice-Chairman Leif RASMUSSEN, Odense Lucyna GRĘBECKA, Warszawa Sergei O. SKARLATO, St. Petersburg Donat-Peter HÄDER, Erlangen Michael SLEIGH, Southampton Janina KACZANOWSKA, Warszawa Jiri VÄVRA, Praha Stanisław L. KAZUBSKI, Warszawa Patricia L. WALNE, Knoxville Leszek KUŹNICKI, Warszawa, Chairman ACTA PROTOZOOLOGICA appears quarterly. The price (including Air Mail postage) of subscription to ACTA PROTOZOOLOGICA at 2000 is: US $ 180,- by institutions and US $ 120,- by individual subscribers. Limited numbers of back volumes at reduced rate are available. TERMS OF PAYMENT: check, money oder or payment to be made to the Nencki Institute of Experimental Biology account: 11101053-3522-2700-1-34 at Państwowy Bank Kredytowy XIII Oddz. Warszawa, Poland. For matters regarding ACTA PROTOZOOLOGICA, contact Editor, Nencki Institute of Experimental Biology, ul. Pasteura 3, 02-093 Warszawa, Poland; Fax: (4822) 822 53 42; E-mail: [email protected] For more information see Web page http://www.nencki.gov.pl/public.htm). Front cover: McQuistion Th. E„ McAllister C.T. and Buice R.E. (1996) A new species of Isospora (Apicomplexa) from captive Pekin robins, Leiothrix lutea (Passeriformes: Sylviidae), from the Dallas Zoo. Acta Protozool. 35: 73-75 ©Nencki Institute of Experimental Biology, Desktop processing: Justyna Osmulska, Data Processing Polish Academy of Sciences Laboratory of the Nencki Institute This publication is supported by the State Committee for Printed at the MARBIS, ul. Kombatantów 60, Scientific Research 05-070 Sulejówek, Poland http://rcin.org.pl Acta Protozool. (2000) 39: 81 - 97 ACTA PR0T0Z00L0GICA Taxonomy and Phylogeny of Heliozoa. I. The Order Desmothoracida Hertwig et Lesser, 1874 Ki.rill A. MIKRJUKOV Department of Zoology and Comparative Anatomy of Invertebrates of Moscow State University, Moscow, Russia Summary. The order Desmothoracida Hertwig et and Lesser, 1874 is reviewed. Five genera and 10 species are recognised: Clcithrulina Cienkowski, 1867 [C. elegans Cienkowski, 1867 and C. smaragdea (Entz, 1877) comb, n.], Hedriocystis Hertwig et Lesser, 1874 [H. pellucida Hertwig et Lesser, 1874, H. minor Siemensma, 1991 and H. zhadani sp. n.], Penardiophrys gen. n. [P. reticulata (Penard, 1904) comb. n. and P. spinifera (Brown, 1918) comb. n.|, Cienkowskya Schaudinn, 1896 [C. mereschkovckii (Cienkowski, 1881) Schaudinn, 1896 and C. brachypous (De Saedeleer, 1930) comb, n.] and Actinosphaeridium Zacharias, 1893 [A pedatus Zacharias, 1893]. The generic names Elaster Grimm, 1872 and Orbulinella Entz, 1877 are synonymised with Clathrulina, and Monomastigocystis De Saedeleer, 1930 with Cienkowskya. The genus Cienkowskya differs from Hedriocystis by an irregular shape of the capsule, and by its attachment to the substrate by a short conical basal region of the capsule rather than by a differentiated tubular stalk as in Hedriocystis. The 2 species of Hedriocystis having a capsule wall composed of polygonal facets are transferred to a new genus Penardiophrys. The genus Actinosphaeridium includes a single freshwater species with branching granule-bearing filopods and the cell body surrounded by a mucus sheath located at the top of a tubular stalk; and is here regarded as a primitive desmothoracid. The first marine Hedriocystis - H. zhadani sp. n. - is described. The stalked heliozoan genus Servetia Poche, 1913 is not included within desmothoracids. Diagnoses of all desmothoracid taxa and a key to 10 species are included. We should look for phylogenetic roots of desmothoracids among heterotrophic biflagellates; cercomonads and gymnosphaerid heliozoa are considered as the most closely related groups to them. Key words: Actinosphaeridium, Cienkowskya, Clathrulina, Desmothoracida, Elaster, fauna, Hedriocystis zhadani sp. n., heliozoa, Orbulinella, Penardiophrys gen. n., phylogeny, Servetia, taxonomy. INTRODUCTION Smith and Patterson (1986) and Patterson (1988, 1994, 1999) that the Heliozoa Haeckel, 1866 are polyphyletic. Recently, we (Mikrjukov 1998, 1999 b, 2000 a, b, c; The Heliozoa is one of the most long-lived of the Mikrjukov et al. 2000) have presented evidence in traditional protozoan taxa. It can be found in the majority favour of the opinion postulated by Tregouboff (1953), of recent systems of protists, protoctists and protozoa (Lee et al. 1985, Karpov 1990, Margulis et al. 1990, Corliss 1994, Hausmann and Hiilsmann 1996, Cavalier- Smith 1998, Kussakin and Drozdov 1998). Heliozoa Address for correspondence: Kirill A. Mikrjukov, Department of Invertebrate Zoology, Faculty of Biology, Moscow State Univer- seem to be comprised of 7-8 mainly distantly related taxa sity, Moscow 119899, Russia; E-mail: [email protected] (Mikrjukov, 1999 b, 2000 a). The heliozoa are therefore http://rcin.org.pl 82 K. A. Mikrjukov to be thought of as members of an adaptive group of 1972). The capsule of the most commonly occurring spherically symmetrical protists with radiating, granule- species, Clathrulina elegans is the only known bearing axopods and lacking any intracellular inorganic palaeonthological (Oligocene) record of heliozoa skeleton and a central capsule (in contrast with another (Deflandre 1953). All the desmothoracid genera are polyphyletic axopodiate group - the radiolaria). An or- normally placed within a single family, Clathrulinidae ganic or inorganic skeleton (if present) is always extra- Claus, 1874, but the group has been ranked up to the cellular (Mikrjukov 1998, 2000 a, b). level of the order. The Desmothoracida Hertwig et Lesser, 1874 ap- Electron microscopical studies of the fine structure of peared in the earliest schemes of classification of heliozoa Clathrulina elegans by Bardele (1971, 1972) and of (Biitschli, 1882; Schaudinn, 1896). The diagnosis and the Hedriocystis pellucida by Brugerolle (1985) have added principle composition of the desmothoracids have re- to our knowledge on this group. They have shown that: mained broadly unchanged despite the disappearance of (i) a the capsule wall has a microfibrillar organic appear- heliozoa as a taxonomic group in recent systems of ance; (ii) their extrusosomes correspond to kinetocysts protists (Lee et al. 2000, Mikrjukov 2000 a). The but their structure does not resemble that of centrohelids taxonomy of various heliozoan taxa is now being re- (Mikrjukov 1995 b); (iii) microtubules in the pseudopods viewed, but this process has yet to extend to the are not ordered in regular axonemal arrays and on this desmothoracids (Roijackers and Siemensma 1988; basis the pseudopods do not comply with the definition of Siemensma and Roijackers 1988 a, b; Siemensma 1991; being axopodia. The fine structure of flagellated swarm- Mikrjukov 1995 a; 1996 a, b; 1997; 1999 c). ers is not well understood but (iv) flagella begin to The order Desmothoracida includes heliozoa enclosed develop from a pair of orthogonally oriented elongated in a (usually) stalked capsule perforated by openings of kinetosomes; (v) the kinetosomes are connected with a various size. Granule bearing, filopods extend out of the front of the nucleus by either an electron-dense these perforations. Sometimes these pseudopodia branch matrix (in Clathrulina) or by a striated rhizoplast off. Cienkowski (1867) was the first to describe a (in Hedriocystis). desmothoracid with his account of Clathrulina elegans. Desmothoracids are traditionally considered to be He noted that only one from of the products of the cell freshwater group of protozoa (Siemensma 1991, the fission remains inside the capsule to remain a heliozoon, taxonomic appendix below). The order has never in- whilst the second one transforms into a distributive cluded a large number of species. The desmothoracids biflagellate swarmer cell, which leaves the capsule have a worldwide distribution, are commonly encoun- through one of the openings in the capsule wall. Further tered, but there is a great variability in the size, shape and investigations (Foulke 1885, Penard 1904, Deflandre ornamentation of the skeleton. Previous workers (Penard 1926, Hoogenraad 1927, Valkanov 1928, De Saedeleer 1904, Rainer 1968, Febvre-Chevalier 1985, Siemensma 1930, Bardele 1972, Brugerolle 1985, Siemensma 1991, 1991) have used taxonomic criteria differently, such that Young et al. 1995) have confirmed the polymorphic there is dispute as to the composition of the group. nature of the life cycle of desmothoracids (Figs. 1 C-F, According to Rainer (1968), the order Desmothoracida K-P, 2 D-G). This includes uni- or biflagellate swarmers, is composed of 4 genera and 8 species: Clathrulina which transform after the settling into
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