Freshwater Heliozoa (Protista, Heliozoa) from Indiana

2003. Proceedings of the Indiana Academy of Science 1 12(2): 169-174

FRESHWATER HELIOZOA (PROTISTA, HELIOZOA) FROM INDIANA

Daniel E. Wujek: Department of Biology, Central Michigan University. Mt. Pleasant. Michigan 48859 USA

ABSTRACT. Six taxa of siliceous scale-bearing heliozoa belonging to the genera Acunthocystis. Fin- aciophora, Pterocystis, Raphidocystis and Raphidiophrys were observed from various nc^rthern Indiana freshwater sites. All are new records for Indiana.

Keywords: Protista, Heliozoa

Previous surveys of Indiana's freshwater scales, the structure of which cannot be dis- protists which utilized electron microscopy cerned clearly by light microscopy. (EM) have reported a diverse flora on the The purpose of this paper is to gi\ e a tax- group of organisms known as the silica-scaled onomic account of Indiana freshwater helio- chrysophytes (Wujek & Swinehart 1995; Wu- zoa observed during EM sur\e\'s for silica- jek & Bechtel 1997). While the taxonomy of scaled chrysophytes (Wujek & Swinehart silica-scale bearing algae of the golden-brown 1995; Wujek & Bechtel 1997) from two north- algae (Chrysophyceae and Synurophyceae) ern counties and Lake Monroe in Monroe has been affirmed on the structure of siliceous County. The only other reports of scaled protists the States using other scales as determined with the electron micro- from United EM than silica-scaled chrysophytes are those oi scope (Takahashi 1978; Asmund & Kristian- Wee & Millie (1983), Wujek et al. (1^)99. sen 1986; Siver 1989; Kristiansen 2002), "the 2002), and Wujek (2003a. b). use of similar criteria in scale-bearing protozoa has been slow to develop" (Nicholls METHODS 1983a). Lugol-fixed plankton samples from a w ide Petersen and Hansen (1960) were the first variety of northern Indiana fresh w aters w ere to describe new species of a group of protis- examined using transmission and scanning tans known as heliozoa based on the electron electron microscopy as previous 1\ described microscopy of their scales. Since 1960 contri- in Wujek & Swinehart (1995) and Wujek c<: butions to the literature on this topic has been Bechtel (1997). Observations were made on samples collected at \arious times l'')^)^ and sporadic. Only the studies of Dtirrschmidt in m 1994: in 1993 from nine sites in Noble Count) Chile, New Zealand and Sri Lanka (1985, (Fig. 1) and one site in Whitnex Coinu\ (Wu- 1987a, b); Nicholls and co-workers in Canada jek & Swinehart 1995): and in U)^)4. 14 sam- (Nicholls 1983a, b; Nicholls & Lynn 1984; ples from Lake Monroe (Wujek \: Becluel Nicholls & Diirrschmidt 1985); Croome and 1997) (Table 1). co-workers in Australia (Croome 1986, 1987a. DISCI SSION b, c; Croome et al. 1987); Siemensma & Roi- OBSERVATIONS AND jackers in The Netherlands (Siemensma 1981; Six species belonging lo ihe helio/oan gen- Siemensma & Roijackers 1988a, b); and Mi- era Accuithocysns. Fiiuiciophnra. Ftcrocysiis. krjukov in Russia (Mikrjukov 1993a, b, Raphidocystis, and Raphidiophrxs were observed from \arious northen Indiana frc->h- 1994a, b, c, 1995, 1996a, b, 1999. 2000a, b) water sites (Table 1. Figs. 2-~). The hclio/oan have demonstrated that scale structure in he- classitication thai follows conforms lo criteria liozoa possessing siliceous scales is the single ). established b\ Page c'v: Siemensma t U^'-M most reliable taxonomic criterion for this group. Previously much of the taxonomy was Crislidiscoid Helio/oa based on light microscopy of variable cell fea- Numerous, but \ariablc round, bicoinex. tures (e.g., color, size, vacuolation, etc.), or of perforated, and o\erlapping scales co\er the

169 —

170 PROCEEDINGS OF THE INDIANA ACADEMY OF SCIENCE

^^^ Meiry Lea Boundary

I I Open Water

L: I Wetland

. Figure 1 —Map of the Merry Lea Environmental Center, showing the location of the sampling sites in Noble County, Indiana.

cells in the genus Pinaciophora. Like all filose 1985), Australia (Croome 1987) and The amoeba, this genus lacks the axonemes and Netherlands and Sweden (Roijackers & Sie- extrusomes observed in the centrohelid helio- mensma 1988). I observed it only once during zoa. my observations (Table 1). Pinaciophora fluviatilis Greeff. (Fig. 2). Centrohelid Heliozoa First reports of this organism for the U.S., un- der the name of Potamodiscus kalbei Gerloff, The genus Acanthocystis contains more were from Mississippi and Ohio (Gaardner et species than any of the other Centrohelida. al. 1976) and Alaska (Manton & Sutherland The genus, erected by Carter (1863), is wide 1979). Gaardner et al. (1976) showed this spe- spread with members occurring in both fresh- cies was incorrectly described as a centric di- water and marine habitats. Cells tend to be atom. It has since been reported from the U.S. round and covered by siliceous spine scales Great Lakes (Wee & Millie 1983) and New with a layer of overlapping body scales.

York (Smol 1987). I observed it from only Acanthocystis polymorpha Diirrsch- one site (Table 1). Other EM reports of this midt.—(Fig. 4). Although scales of this or- species include both marine and freshwater ganism were originally illustrated by Taka- habitats in Europe (Thomsen 1978; Belcher & hashi (1959) as occurring in Japan, it was not Swale 1978), Canada (Nicholls 1983b), Ant- until 1985 that Durrschmidt (1985) formally arctica (Takahashi 1981), and The Netherlands described it as a taxon from Chile. Its occur- (Roijackers & Siemensma 1988). rence in Indiana (Table 1) represents the sec- Raphidiophrys intermedia Penard.—(Fig. ond report for this species in the U.S. 3). The cells of the genus Raphidiophrys are Pterocystis fortesca (Nicholls) Siemensma coated with curved, spindle-shaped scales. & Roijackers.—(Fig. 5). Members of the ge- Eighteen species are recognized (Mikrjukov nus Pterocystis (Siemensma & Roijackers 1994c). The only EM reports of this species 1988a), as in the genus Choanocystis, possess are from Canada (Ontario), Chile, New Zea- tangential plate scales and radial spine scales. land and Malaysia (Nicholls & Durrschmidt However, the spine scales are bilaterally sym- )

WUJEK—INDIANA HELIOZOA 17]

Figures 2-7.—Transmission electron micrographs of siliceous scales of Indiana liclio/oans. 2. Pinacio- phora fluviatilis, plate scale; 3. Raphidiophrys intermedia, lamellate plate scale: 4. Accinfhccvstis />('/v- morpha, cell with plate and spine scales; 5. Pterocystis forresca, spine scale: 6. A\//'///t/('c \ vr/v mhiuni, plate scale, two large plate scales; 7. Raphidocystis flabellata, circuhu- plate scale. Scale bars = 1 ijim.

1. Table —Indiana locations containing heliozoa. See Wujek c^ Swinehari [ l'-)'^)5) and Wujok A; Hi (1997) for physiochemical data.

Taxon Date Localioii

Acan thocystis polymorplia 4 May 1994 Lake Monroe (Monroe C\nint\ i

Pinaciophora fluviatilis 28 June 1994 Lake Monroe (Monioc C\nini\ i

Pterocystis fortesca 29 June 1993 Crooked lake i\\ hule> C\nim\ >: Ke Img Pond.

High Lake .<: Reilh Cua\cl Pu iNo le e\nint\

8 June 1994 Lake Monroe i Monroe C\nini\ '

> Raphidocystis fioheUata 2 July 1993 Lealherleaf Bog i Noble C\nini\

Raph idocystis tub ifera 29 June 1993 Reith Gravel Pit .v^ raniaraek Bog

2 July 1993 Leatherleaf Bog lall Noble (.\nini> ^

Rap/i idioph rys if iteniiedia 2 July 1993 Leatherleaf Boe (Noble Couiu\ i 172 PROCEEDINGS OF THE INDIANA ACADEMY OF SCIENCE

metrical, with a cylindrical shaft and membra- Monroe samples, P. Eisner for preparing the nous base which merge into two lateral mem- carbon-coated grids, and G. Williams and A. branous wings that extend for some distance Weber for assistance in the preparation of the along the shaft. photographic plate. This study was in part Originally described from Canada as Acan- funded through a grant from the CMU FRCE thocystis fortesca Nicholls (1983a), Siemens- committee. ma & Roij ackers (1988a) transferred it to the genus Pterocystis and also placed it in syn- LITERATURE CITED with the taxon Acanthocystis panto- onymy Asmund, B.C. & J. Kristiansen. 1986. The genus podecoides Nicholls (1983a). It has since been Mallomonas. Opera Botanica 85:1-128. reported from Australia (Croome 1986). This Belcher, J.H. & E.M.E Swale. 1978. Records from species was the most widely observed in this England of the heliozoan-like organism Pinacio- study (Table 1). phora fluviatilis Greeff and of its scales, ''Pota- Raphidocystis flabellata (Diirrschmidt) modiscus kalbeV Gerloff. Archiv fiir Protisten- kunde 120:367-378. Page & Siemensma.—(Fig. 7). Species in the Carter, H.J. 1863. On a freshwater species Echin- genus Raphidocystis tend to have cells that are ocystidia, Acanthocystis tujfacea, n. sp. et gen.? round and covered with cup-shaped scales in Annual Magazine of Natural History 12:262- addition to many radiate tubular scales. Pre- 264. viously reported from Chile, New Zealand, Croome, R.L. 1986. Observations of the heliozoan Germany, and Canada (Diirrschmidt 1987), it genera Acanthocystis and Raphidocystis from has been recently reported from the Gulf Australia. Archiv fiir Protistenkunde 131:189-

Coast of the U.S. (Wujek 2003b). I observed 199. it only from the Leatherleaf bog sample (Table Croome, R.L. 1987a. Observadons of the genera Acanthocystis, Raphidiophrys, Clathrulina and 1). Pompholyxophrys (Protozoa, Sarcodina) from Raphidocystis tubifera Penard.—(Fig. 6). Australian freshwaters. Archiv fiir Protistenkun- Since its original description from France de 133:237-243. (Penard 1904), electron microscopic reports of Croome, R.L. 1987b. Pinaciophora ovalis (Rotos- this species include: Rees et al. from (1980) phaerida, Heliozoea), a new species from Aus-

England and Canada; Nicholls & Diirrschmidt tralia. Archiv fiir Protistenkunde 134:343-346. (1985) from Canada, Chile, New Zealand, Croome, R.L. 1987c. Pinaciophora columna n. sp., Malaysia and Sri Lanka; Croome (1986) from P. tasmanica n. sp. and P. apora n. sp., new Australia; Finlay et al. (1988) from England; heliozoeans from Australia, and a report of P. and Wujek (2003b) from the United States fluviatilis Greeff from Antarctica. Archiv fiir Protistenkunde 133:15-20. based on studies using EM. I observed it in Croome, R.L., J. van den Hoff & H.R. Burton. collections from three sites (Table 1). 1987. Observations of the heliozoean genera Unidentified Scales Pinaciophora and Acanthocystis (Heliozoa, Sar- codina, Protozoa) from Ellis Fjord, Antarctica. The short species list given above is not Polar Biology 8:23-28. exhaustive. I observed a number of other Durrschmidt, M. 1985. Electron microscopic ob- scales, but I was unable to identify them be- servations on scales of species of the genus cause in most cases either the plate or spine Acanthocystis (Centrohelidia, Heliozoa) from scales were not present and both are usually Chile, I. Archiv fur Protistenkunde 129:55-87. needed to confirm identifications. Diirrschmidt, M. 1987a. An electron microscopical

What is significant is the paucity of taxa study of freshwater heliozoa (genus Acanthocys- observed when considering that 24 different tis, Centrohelidia) from Chile, New Zealand, sampling sites were sampled. Collections and Malaysia and Sri Lanka. II. Archiv fiir Protisten- kunde 133:49-80. observations representing other seasons and Diirrschmidt, M. 1987b. An electron microscopical from other regions will undoubtedly yield ad- study of freshwater heliozoa (genus Acanthocys- ditional species. tis, Centrohelidia) from Chile, New Zealand, ACKNOWLEDGMENTS Malaysia and Sri Lanka. III. Archiv fiir Profis- tenkunde 133:21-48. I would like to thank M. Wujek and Dr. A. Finlay, B.J., K.J. Clarke, A.J. Cowling, R.M. Hin- Swinehart for assistance in the field. Dr. dle & A. Rogerson. 1988. On the abundance and

Swinehart for Fig. 1 , G. Bechtel for the Lake distribution of Protozoa and their food in a pro- WUJEK—INDIANA HELIOZOA 173

ductive freshwater pond. European Journal of Nicholls, K.N. 1983a. Little-kn(n\n and nev-v helio- Protistology 23:205-217. zoeans: the centrohelid genus Acanthocystis, in- Gaardner, K.R., G.A. Fryxell & G.R. Hasle. 1976. cluding descriptions of nine new species. Cana- Potamodiscus kalbei Gerloff - an organism with dian Journal of Zoology 61 : 1 369-1 386. siliceous scales. Archiv fur Protistenkunde 118: Nicholls, K.N. 1983b. Little-known and ntw helio-

346-351. zoeans: Pinaciophora trian^ula Thomscn nev*. to Kristiansen, J. 2002. The genus Mallomonas (Syn- North America and a description of Pinaciopho- urophyceae) - A taxonomic survey based on the ra pinea sp. nov. Canadian Journal of Zoology ultrastructure of silica scales and bristles. Opera 61:1387-1390. Botanica 139:1-218. Nicholls, K.N. & D.H. Lynn. 1984. Lepidoirach- Manton, I. J. Sutherland. 1979. Further obser- & elophylliim foniicis n. g., n. sp.. a cilialc \\\\Y\ an vations on Potamodiscus = Gerloff Pinaciopho- external layer of organic scales (Ciiiophora. Li- ra Greeff, with species to reference Alaska and tostomatea, Haptoria). Journal of Protozoology Arctic Canada. Journal of the Linnean Society of 31:413-419. London, Zoology 67:285-295. Nicholls, K.N. & M. Durrschmidl. 1985. .Scale Mikrjukov, K.A. 1993a. Observations on Centro- structure and taxonomy of some species of Ra- heliozoa of the Volga basin (Protozoa: Sarcodi- phidocystis, Raphidiophrys, and Pompholyxo- na). Zoosystmatica Rossica 2:201-209. phrys (Heliozoea) including descriptions of six Mikrjukov, K.A. 1993b. On the centrohelid and ro- new taxa. Canadian Journal of Zoolog\ 63: tosphaerid heliozoa from the environs of the 1944-1961. Vortsjarv Limnological Station in Estonia. Pro- Page, EC. & EJ. Siemensma. 1991. Nackte Rhi- ceedings of the Estonian Academy of Science zopoda und Heliozoea. Gustax Fischer \erlag. 42:154-160. Stuggart. 297 pp. Mikrjukov, K.A. 1994a. Marine and brackish- wa- Penard, E. 1904. Les Heliozoaires d'eau douce. ter centrohelids (Centroheliozoa, Sarcodina) of Geneve. 341 pp. Kandalaksha Bay of the White Sea. Zoology Petersen, J. P. & J.B. Hansen. 1960. Electronenmi- Journal 73:5-17. (in Russian) kroskopische Untersuchungen \on zwei der He- Mikrjukov, K.A. 1994b. Observations of Centro- liozoen-Gattung Actinocystis. .Archix fiir Protis- heliozoa from Moscow marine aquaria. Archiv tenkunde 104:547-553. fur Protistenkunde 144:450-455. Rees, A.J., D.A. Donaldson & G.E Leedale. l^iSO. Mikrjukov, K.A. 1994c. Rabdiophrys pertzovi sp. Morphology of the scales of the freshw ater he- nov.- a new marine rotosphaerid heliozoon from liozoan Raphidocystis rubifera (Heliozoa. Cen- the White Sea. Archiv fiir Protistenkunde 144: trohelida) and organization of the intact scale 325-327. layer. Protistologica 16:565-570. Mikrjukov, K.A. 1995. Revision of the species Roijackers. R.M.M. & EJ. Siemensma. l^SS. .A composition of the genus Choanocystis (Sarco- study of cristidiscoidid amoebae (Rhi/opoda. Fi- dina, Centroheliozoa) and its fauna in eastern Eu- losea) with description of new species and kc\ s rope. Zoology Journal 54:3-16. to genera and species. .A.rchi\- fiir Protistenkunde Mikrjukov, K.A. 1996a. Revision of the genera 135:237-253. and species composition of lower Centrohelio- Siemensma, EJ. 1981. De Nedcrlandsc Zonnedi- zoa. I. Family Heterophryidae Poche. Archiv fiir ertjes (Actinopoda. Hclio/oa). W'etcnschappcl- Proti stenkunde 147:107-113. ijke Koninklijke NcderlandNC Na- Mikrjukov, K.A. 1996b. Revision of genera and Mededelingen tuurhistorische Vereniging U'^);!-! IS. species composition of lower Centroheliozoa. II. EJ. Roijackers. l^\^Sa. Family Raphidiophryidae. Archiv fur Protisten- Siemensma. & R.M.M. A kunde 147:205-212. study of new and little-known acanihocx slid hc- Mikrjukov, K.A. 1999. Taxonomic revision of liozoeans. and a proposed k.\\\ ision ot' the genus scale-bearing heliozoan-like amoebae (Pompho- Acantliocystis (Actinopoda. Hclio/ocat. .-\rchi\

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Species of Acanthoecidae and the Centrohelida chrysophytes from Indiana. II. Proceedings of found at a site selected on fast ice. Antarctic Re- the Indiana Academy of Science 106:291-298. cord 73:1-22. Wujek, D.E., D.M. Schmidt & J.L. Cook. 1999. Thomsen, H.A. 1978. On the identity between the First report of Lepidotrachelophyllum fornicus heliozoan Pinaciophora fliiviatilis and Potamo- Nicholls and Lynn in the United States. Journal discus kalbei with the description of eight new of the Elisha Mitchell Scientific Society 115: Pinaciophora species. Protistologica 24:359- 319-321. 373. Wee, J.L. & D.E Millie. 1983. A new record of Manuscript received 16 April 2003, revised 4 Pinaciophora fliiviatilis Greeff sensii Penard September 2003.