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Parvodinium gen. nov. for the Umbonatum Group of Peridinium (Dinophyceae).

ABSTRACT: Peridinium is a genus of freshwater thecate dinoflagellate. Because it was one of the earliest named genera (Ehrenberg 1832), many species placed in it were later removed to other genera. Genera continue to be extracted and Peridinium, while more closely defined, still harbors groups of species unlike the type species, P. cinctum. It is the goal of this paper to remove one of the most dissimilar groups, the Umbonatum Group. Peridinium cinctum has no apical pore, three apical intercalary plates and five cingular plates. Species in the Umbonatum Group have an apical pore, two apical intercalary plates and six cingular plates warranting their separation into a new genus, Parvodinium.

INTRODUCTION

Freshwater dinoflagellates are a group of algae found mostly in open water habitats. As members of the phytoplankton they are food for zooplankton and may form blooms during the temperate summer. Most are recognizable as dinoflagellates by their golden brown color and shape, but further taxonomic identity may be challenging. Many reports of dinoflagellates, as part of a list of taxa, include only "Peridinium sp." The genus Peridinium was originally established for cells with a cell wall divided into plates and with a transverse groove (Fig. 1), and was distinguished from a similar genus (Glenodinium) by the absence of an eyespot (Ehrenberg 1830, 1838). Stein (1883) refined the description by illustrating the plate tabulation pattern of P. cinctum (O.F.Muller) Ehrenberg, the type species (Fig. 2). It has long been recognized that species in Peridinium showed a great deal of variability. 3-hecate dinoflagellate taxa are primarily defined by the number and arrangement ofplates in the epitheca, hypotheca, sulcus and cingulum, the latter three considered more conservative (Balech 1980). Balech (1974) used differences in the number and shape of cingular plates to separate Protoperidinium from Peridinium, and other taxa first described as species of Peridinium have been moved to other genera including Gymnodinium, Gonyaulax, Ceratium, irhompsodinium and Glochidinium based on differences from the plate pattern of P. cinctum. Peridinium has come to be defined as having a plate formula of 4' 2-3a, 7", 5'" 2'"', with species based on the presence/absence of an apical pore, the two alternatives for number of apical intercalary plates, plate arrangements, size, ornamentation, and nutrition (photosynthetic or heterotrophic). Peridinium species have longbeen organizedinto groups based these features. Lemmermann (1910) had a section Poroperidinium (with an apicalpore) and Cleistoperidinium (without),Lindemann (1918) had Gruppe: Peridinium willei, and Gruppe: Peridinium cinctum, in addition to species in Poroperidinium. Lefevre's monograph (1932) divided Peridinium into subgenus Cleistoperidinium (with Groupes Willei, Striolatum, Cinctum, and Palatinum) and subgenus Poroperidinium (with Groupes Bipes, Gutwinskii, Umbonatum, Elpatiewskyi, Cunningtonii, Lindemanni, Penardi, Lomnickii, Godlewskii, Allorgei, and Polonicum). Many of the species groups in Poroperidinium are now in the genus Peridiniopsis (3-5', 0-1a,6-8", 5'", 2'"')(Bourrelly 1968). Popovslo) and Pfiester (1990) continued dividing Peridinium into two subgenera Poroperidinium and Cleisotoperidinium with the same four sections in Cleistoperidinium and five sections in Poroperidinium. Groupe Cinctum, in subgenus Cleistoperidinium, includes the type species, Peridinium cinctum (O.EMuller) Ehrenberg, which lacks an apical pote and has three apical intercalary plates in an asymetrical arrangement. It has been suggested that ali species differing from the type species should not be considered Peridinium (Fensome and others 1993). Groupe Umbonatum, in subgenus Poroperidinium, has an apical pore and two apical intercalary plates. Examination of these and other features contrasting the species in the Umbonatum Group with Peridinium cinctum provides sufficient morphological evidence to remove them from Peridinium and place them into a new genus. The genus Parvodinium gen. nov. is proposed to accommodate one obviously distinct group from the genus Peridinium.

MATERIALS AND METHODS

Samples have been collected from the United States, Belize and Ecuador. I have collected Peridinium cinctum twice, and only its forms; form meandricum Lefevre from Texas and form tuberosum (Meunier) Lindemann from Ohio. Peridinium gatunense Nygaard, which has the same plate pattern and can be mistaken for P. cinctum (Hickel and Pollingher 1988), is common and has been collected from Michigan (MI), Minnesota (MN), North Carolina (NC), Ohio (OH), Texas (TX), Washington (WA), and Wisconsin (WI). Peridinium umbonatum has been collected from Florida (FL), NC, OH, TX, WA, P. africanum from TX, P. belizensis from Belize, P. centenniale from Belize, P. inconspicuum from TX, OH, WA, MI, WI and Wyoming and P. goslaviense from OH. Plate designation follows Kofoid (1909). Plate details have been reconstructed from scanning electron microscope (SEM) images taken with a Hitachi S-2700.

RESULTS AND DISCUSSION

Peridinium cinctum has a plate pattern of four apical, three apical intercalary and seven precingular plates in the epitheca, there is no apical pore, the 1' plate does not reach the apex, the 3' plate is topmost, the 2' plate is moderately sized, the 3' and 4' are large (Fig. 3a-c). The apical intercalaryplates are described as asymmetrical (to contrast with the symmetrical apical plates of the Willei Group), there is a small, pentagonal la, larger 2a, and large 3a plate (Fig. 3c). In dorsal view, the 4" plate is central and five sided, the 2a and 3a plates both touching it (Fig. 3b). Antapical plates are about equal in size (Fig. 3d). There are five cingular plates aligned with the postcingulars (Fig. 1e) and five sulcal plates (Fig. 3f). Thecal plates are thick, frequently have reticulate ornamcntation, and cells are large, 40-64[micro]m diameter (Table 1).

The Cinctum group contains two species besides P. cinctum, they share the asymmetry of the apical plates and differ in overall shape. Peridinium gatunense Nygaard is spherical with no dorsoventral compression, has wide cingular lists and a small first apical plate. Peridinium raciborskii Woloszynskais large (70-80Fm), and strongly dorsoventrally compressed. Peridinium cinctum has some named variations.

Peridinium umbonatum Stein (Fig. 4-5) has a plate pattern of four apical, two apical intercalary and seven precingular plates in the epitheca, there is an apical pore covered by a cover plate and surrounded by a pore plate, and a canal plate runs ventrally to the apex of the 1' plate (Figs. 5a-c, 6, 8). Antapical plates are about equal in size (Fig. 5d). The six cingular plates are not neatly aligned with pre- or postcingularplates except for the mid dorsal alignment of all three (Fig. 5e). Sulcai plates differ individually from their counterparts in P. cinctum, especially the Sd in P. umbonatum which forms a distinctive flap over the flagellar pore (Figs. 5f, 6). On the dorsal surface the two apical intercalary plates, and the 3' and 4" plates have a plastic relationship, conjunctum when the 3' and 4" share a suture and 1a and 2a are separated (Figs. 5b, c, 7, 8, and in original Stein drawings Fig. 4), contactum when all four plates meet (Fig. 5g), and remotum when 1a and 2a share a suture and 3' and 4" are separated (Fig. 5h)(Lefevre 1932). Lefevre (1932)included the dorsal plate arrangement (ie Peridinium umbonatum tab. conjunctum) as part of the species name. Work on clonal isolates shows all three forms may appear, though 94% were conjunctum, and that in natural populations either conjunctum or remotum may predominate (Elrachter and Meyer 2001). Plate fluidity is characteristic of some taxalike the species in the Umbonatum Group, Thompsodinium (Carty 1989), and Durinskia (Chesnick and Cox 1985). In the Umbonatum Group thecal plates are thinner than in the Cinctum group, there are various types of omamentation, cells are small (12-20 [micro]m diameter), and forms/varieties often have spines (Table 1).

[FIGURES 1-3 OMITTED]

Species within the Umbonatum group are distinguished by overall shape, presence of spines, and plate sizes and positions. Popovsky and Pfiester (1986, 1990) synonomized many species with P. umbonatum (retaining P. morzinense and P. africanum) as varieties (var. centenniale, var. deflandrei, var. goslaviense, var. lubieniense and var umbonatum). Much of the perceived overlap among the species can be eliminated by reference to original descriptions and illustrations.

[FIGURES 4-5 OMITTED]

Sexual reproduction has been investigatedin P. cinctum (Pfiester 1975) and P. inconspicuum in the Umbonatum Group (Pfiester and others 1984). While there are many similarities, P. inconspicuum was unique among Peridinium species in having the gamete protoplasts leave their thecae and fuse in the middle (Pfiester and others 1984).

Molecular analyses of species using small subunit (SSU) ribosomal RNA generates phylogenetic trees that show some clades of Peridinium species (P. volzii, P. willei, P. bipes) distant from "Peridinium" umbonatum (Saldarriaga and others 2004). A more extensive phylogenetic analysis using both SSU and large subunit (LSU) data, and focused on freshwater species, also found a group of Peridinium species (P. cinctum, P. bipes, P. gatunense, P. volzii, P. willei) separated from Umbonatum group species (umbonatum, inconspicuum, centenniale) (Logares and others 2007). These two studies add credence to the separation of the Umbonatum group from Peridinium.

Parvodinium Carty genus novum Dinoflagellatum aquae dulcis, ovatae ad quinqueangulatus, theca tenue, ordinatione tabulari Po, 4', 2a, 7", C6, S5, 5'", 2"", chromatophoris aureus, epitheca hypothcamsuperantia, cingulum latum.

Freshwater dinoflagellate, small, ovoid topentagonalcell, plates thin, plate pattern: apical pore, pote plate, canal plate, 4', 2a, 7", C6, S5, 5"', 2"", most photosynthetic with yellow-gold plastids, cingulum is wide, sub-median and the hypotheca is smaller than the epitheca. Most species the sulcus enters the epitheca and spreads to the antapex; 3' and 4" plates may be in conjunctum, contactum or remotum positions.

Type species: Parvodinium umbonatum (Stein) Carty comb. nov. Etymology: parvo (L) small, din whirling

Parvodinium africanum (Lemmermann) Carty comb. nov. Basionym: Peridinium africanum Lemmermann ex West 1907 J. Linn. Soc. Bot. 38:188 P19 1a-e.

Parvodinium belizensis (Carty) Carty comb. nov. Basionym: Peridinium belizensis Carty ex Carty and Wujek 2003. Carib. J. Sci. 39:137, Fig 14.

Parvodinium centenniale (Playfair) Carty comb. nov. Basionym: Peridinium umbonatum var centenniale Playfair 1919. Proc. Linn. Soc. N.S.W. 44:806 Text fig 14.

Parvodinium deflandrei (Lefevre) Carty comb. nov. Basionym: Peridinium deflandrei Lefevre 1927. Bull. Mus. Hist. Nat. Paris 33:121

Parvodinium goslaviense (Wotoszynska) Carty camb. nar. Basionym: Peridinium gaslaviense Wotoszynska 1916. Bull. Acad. Sci. Cracovie Ser. B. p267 Taf 10, Fig 18-24.

Parvodinium incanspicuum (Lemmermann) Carty cama nov. Basionym:Peridinium inconspicuum Lemmermann 1899. Abh. Nat. ver. Breman, XVI p350

Parvodinium lubieniense (Woloszynska) Carty comb. nov. Basionym: Peridinium lubieniense Woloszynska 1916 Bull Acad. Sci. Cracovie Ser. B p272, Taf 12, Fig 21-24.

Parvodinium morzinense (Lefevre) Carty comb. nov. Basionym: Peridinium morzinense Lefevre 1928. Annales de Protistol., I. p137 Peridinium elegans Lefevre 1925 Rev. Algol. 2:332-333.

Parvodinium pusillum (Penard) Carty comb. nov. Basionym: Glenodinium pusillum Penard 1891. Bull. trav. Soc. Bot. Geneve VI p52-53 P1 IV Figs 1-4.

Parvodinium umbonatum (Stein) Carty comb. nov. Basionym: Peridinium umbonatum Stein 1883 Organ. Infus. III P1 XII Figs 1-8
Key to the species of Parvodinium

1a. Cell lacking plastids, P. goslaviense
single slender antapical spine

1b. Cell with plastids 2

2a. Epitheca hemispherical, P. centenniale
 apical pore off-center

2b. Epitheca angular, pore central, 3
 cingulum median

2c. Epitheca rounded, pore central 5

3a. Cell with 2 prominent P. deflandrei
 hypothecal spines

3b. Cell with small spines or none 4

4a. Small stout spine(s) on hypotheca P. africanum

4b. Small spines, if any P. inconspicuum

5a. Plate margins curved P. morzinense

5b. Plate margins straight 6

6a. Sulcus expanding to P umbonatum
 antapex, epitheca > hypotheca

6b. Sulcal margins parallel or little expanded 7

7a. Antapical plates unequal P belizensis

7b. Antapical plates equal in size 8

8a. Epitheca > hypotheca, 13-20 [micro]m long P. pusillum

8b. Epitheca [approximately equal to] P lubieniense
 hypotheca, 35-45 [micro]m long


[FIGURES 6-8 OMITTED]

Most of the other groups currently in Peridinium also differ morphologically from the Cinctum group, however, most have three intercalaryplates. The Palatinium Group (Lefevre 1932), including P palatinium and P pseudolaeve, was placed in Cleistoperidinium with the Cinctum Group since it lacked an apical pote, but is a separate group since it has two apical intercalary plates. At this time I am not removing these species into Parvodinium since LSU rDNA closely linked P cinctum and Ppseudolaeve (Daugbjerg and others 2000).

ACKNOWLEDGEMENTS. The author wishes to thank Nancy Rubenstein, reference librarian at Heidelberg University, for her help in tracking down original citations; Heiddberg University for Aigler grants which supported this work, the electron microscopy center at Bowling Green State University in Ohio for use of their SEM, and Tara Ensing for help with images.

LITERATURE CITED

Balech E. 1974. El genero Protoperidinium Bergh, 1881 (Peridinium Ehrenberg, 1831,partim). Revista del Museo Argentino de Ciencias Naturales <<Bernardino Rivadavia" IV, No 1. Buenos Aires.

Balech E. 1980. On thecal morphology of dinoflagellates with special emphasis on circular (sic) and sulcal plates. An. Centro Cienc. del Mar y Limnol. Univ. Nal. Auton. Mexico 7: 57-68.

Boltovskoy A. 1975. Estructura y estereoultraestructura tecal de dinoflagelados. II. Peridinium cinctum (Muller) Ehrenberg. Physis secc. B. Buenos Aires 34:73-84.

Bourrelly P. 1968. Note sur Peridiniopsis borgei Lemm. Phykos 7:1-2.

Carty S. 1986. The taxonomy and systematics of freshwater armored dinoflagellates. Ph.D. dissertation. Texas A&M Univ. College Sta. TX 286pp.

Carty S. 1989. Thompsodinium and two species of Peridiniopsis (Dinophyceae): taxono mic notes based on scanning electron micrographs. Trans. Am. Microsc. Soc. 108:64-73.

Carty S, Wujek DE. 2003. A new species of Peridinium and new records of Dinoflagellates and silica-scaled Chrysophytes from Belize. Carib. J. Sci. 39:136-139.

Chesnick JM, Cox ER. 1985. Thecal plate tabulation and variation in Peridinium balticum (Pyrrhophyta: Peridiniales). Trans. Am. Microsc. Soc. 104:387-394.

Daugbjerg N, Hansen G, Larsen J, Moestrup O. 2000. Phylogeny of some of the major genera of dinoftagellates based on ultrastructure and partial LSU rRNA sequence data, including the erection of three new genera of unarmoured dinoflagellates. Phycologia 39:302-317.

Ehrenberg CG. 1830 (1832). Beitrage zur Kennmis der Organisation der Infusorien and ihrer geographischen Verbreitung, besonders in Sibirien. Abh. Konigl. Akad. Wiss. Berlin.

Ehrenberg CG. 1838. Die Infusionsthierchen als volkommene Organismen. Berlin und Leipzig.

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Fensome RA, Taylor FJR, Norris G, Sarjeant WAS, Wharton DI, Williams GL. 1993. A classification of living and fossil dinoflagellates. Micropaleontology Spec. Publ. 7. 351pp

Hickel B, Pollingher U. 1988. Identification of the bloom-forming Peridinium from Lake Kinnetet (Israel) as P. gatunense (Dinophyceae). Br. Phycol. J. 23:115-119.

Kofoid CA. 1909. On Peridinium steini Jorgensen, with a note on the nomenclature of the skeleton of the Peridinidae. Archiv fur Protistenk. 16:25-47

Lefevre M. 1925. Contribution a la flore des Peridiniens de France. Rev. Algol. 2:327-342.

Lefevre M. 1927. Sur les variations tabulaires chez les Perininiens d'eau douce et leur notation. Diagnoses d'especes et de varietes nouvelles. Bule Mus. Hist. Nat. Paris 33:118-122.

Lefevre M. 1928. Peridinium morzinense nem. nov. Ann. de Protistol., I. p137.

Lefevre, M. 1932. Monographie des especes d'eau douce du genre Peridinium. Arch. Bot. Mem. Caen 2: 1-208.

Lemmermann E. 1899. Ergebnisse einer Reise nach dem Pacific (H. Schauinsland 1896/97). Planktoalgen. Abh. Nat. Ver. Breman Bd XVI P313-398 P11-3.

Lemmermann E. 1910. Kryptogamenflora der Mark Brandenburg, III, Algen I. Gebruder Borntraeger, Leipzig. pp. 497-712.

Lindemann E. 1918. Untersuchungen uber Susswasserperineen und ihre Variationsformen II. Archiv fur Naturgeschichte 1918 A 8:121-194.

Logares R, Shalchian-Tabrizi K, Boltovskoy A, Rengefors K. 2007. Extensive dinoflagellate phylogenies indicate infrequent marine-freshwater transitions. Molecular Phylogenetics and Evolution 45:887-903.

Penard E. 1891. Les Peridiniacees du Leman. Buli trav. Soc. Bot. Geneve VI :52-63.

Pfiester LA. 1975. Sexual reproduction of Peridinium cinctum f. ovoplanum (Dinophyceae). J. Phycol. 11:259-265.

Pfiester LA, Timpano P, Skvarla JJ, Holt JR. 1984. Sexual reproduction and meiosis in Peridinium inconspicuum Lemmermann (Dinophyceae). Amer. J. Bot. 71:1121-1127.

Playfair GI. 1919. Peridineae of New South Wa]es. Proc. Linn. Soc. NSW 44:793-818.

Popovsky J, Pfiester LA. 1986. A taxonomical note to the Section umbonatum of the genus Peridinium Ehrenberg, 1932 (Dinophyceae). Arch. Protistenkd. 132:73-77.

Popovsky J, Pfiester LA. 1990. Susswasserflora von Mitteleuropa. Band 6: Dinophyceae (Dinoflagellida). Gustav Fischer Verlag, Jena. 272 pp.

Saldatriaga JF, Taylor FJR, Cavalier-Smith T, Menden-Deuer S, Keeling PJ. 2004. Molecular data and the evolutionary history of dinoflagellates. European Journal of Protistology 40:85-111.

Stein FR. 1883. Der organismus der Infusionsthiere. Abt. III Verlagvon Wilhelm Engdmann, Lcipzig.

West G S. 1907. Report on the freshwater algae, including phytoplankton, of the Third Tanganyika Expedition conducted by Dr.W.A. Cunnington, 1904-1905. Linn. J. Bot. 38:81-195, 10 plates.

Wotoszynska J. 1916. Polnische Susswasser-Peridineen. Bull Acad. Sc. Cracovie Cl. Math. Nat. Ser. B. Sc. Nat. 260-285 P110-14.

SUSAN CARTY, Department of Biological and Environmental Science, Heidelberg University, Tiffin, OH

Address correspondence to Susan Carty, Department of Biological and Environmental Science, Heidelberg University, Tiffin, OH 44883. Email: scarty@ heidelberg.edu
TABLE 1
Differences between Peridinium cinctum and
Parvodinium umbonatum

Feature Peridinium Parvodinium
 cinctum umbonatum

# apical intercalary plates 3 2
# cingular plates 5 6
Size-length 40-64[micro]m 16-28[micro]m
Size-width 33-58[micro]m 12-26[micro]m
Apical pore no yes
Hypothecal spines no sometimes
Sulcusin hypotheca parallel sides widely spreading
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Date:Dec 1, 2008
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