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

Peridinium is a genus of freshwater thecate dino¢ agellate. 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 de› ned, 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 › ve 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. OHIO J SCI 108 (5): 103-107, 2008 INTRODUCTION Freshwater dinoÈ agellates 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 dinoÈ agellates by their golden brown color and shape, but further taxonomic identity may be challenging. Many reports of dinoÈ agellates, as part of a list of taxa, include only “Peridinium sp.” ̈ e 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) re¬ ned the description by illustrating the plate tabulation pattern of P. cinctum (O.F.Müller) Ehrenberg, the type species (Fig. 2). It has long been recognized that species in Peridinium showed a great deal of variability. ̈ ecate dinoÈ agellate taxa are primarily de¬ ned by the number and arrangement of plates in the epitheca, hypotheca, sulcus and cingulum, the latter three considered more conservative (Balech 1980). Balech (1974) used di3 erences in the number and shape of cingular plates to separate Protoperidinium from Peridinium, and other taxa ¬ rst described as species of Peridinium have been moved to other genera including Gymnodinium, Gonyaulax, Ceratium, ompsodinium and Glochidinium based on di3 erences from the plate pattern of P. cinctum. Peridinium has come to be de¬ ned as having a plate formula of 4ʹ 2-3a, 7ʹʹ, 5ʹʹʹ 2ʹʹʹʹ, 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 long been organized into groups based these features. Lemmermann (1910) had a section Poroperidinium (with an apical pore) and Cleistoperidinium (without), Lindemann (1918) had Gruppe: Peridinium willei, and Gruppe: Peridinium cinctum, in addition to species in Poroperidinium. Lefèvre’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 (3-5ʹ, 0-1a, 6-8ʹʹ, 5ʹʹʹ, 2ʹʹʹʹ)(Bourrelly 1968). Popovský and P¬ ester (1990) continued dividing Peridinium into two subgenera Poroperidinium and Cleisotoperidinium with the same four sections in Cleistoperidinium and ¬ ve sections in Poroperidinium. Groupe Cinctum, in subgenus Cleistoperidinium, includes the type species, Peridinium cinctum (O.F.Müller) Ehrenberg, which lacks an apical pore and has three apical intercalary plates in an asymetrical arrangement. It has been suggested that all species di3 ering 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 suμ cient morphological evidence to remove them from Peridinium and place them into a new genus. ̈ e 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 Lefèvre 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. a icanum 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 1ʹ plate does not reach the apex, the 3ʹ plate is topmost, the 2ʹ plate is moderately sized, the 3ʹ and 4ʹ are large (Fig. 3a-c). ̈ e apical intercalary plates are described as asymmetrical (to contrast with the symmetrical apical plates of the Willei Group), there is a small, pentagonal 1a, larger 2a, and large 3a plate (Fig. 3c). In dorsal view, the 4ʹʹ plate is central and ¬ ve sided, the 2a and 3a plates both touching it (Fig. 3b). Antapical plates are about equal in size (Fig. 3d). ̈ ere are ¬ ve cingular plates aligned with the postcingulars (Fig. 1e) and ¬ ve sulcal plates (Fig. 3f ). ̈ ecal plates are thick, frequently have reticulate ornamentation, and cells are large, 40-64μm diameter (Table 1). ̈ e Cinctum group contains two species besides P. cinctum, they share the asymmetry of the apical plates and di3 er in overall shape. Address correspondence to Susan Carty, Department of Biological and Environmental Science, Heidelberg University, Tiμ n, OH 44883. Email: scarty@ heidelberg.edu 104 VOL. 108 UMBONATUM GROUP OF PERIDINIUM Figures 1-3. Line drawings. Fig. 1. Original drawing from Ehrenberg 1830. Fig. 2. Diagram from Stein (1883) showing plates. Fig. 3a. Ventral view, one plate showing reticulate ornamentation. Fig.3b. Dorsal view, plates numbered using Kofoidian system. Fig. 3c. Apical view with plates identi¬ ed, note asymmetrical arrangement of apical and apical intercalary plates. Fig. 3d. Antapical view. Fig. 3e. Cingular plates with sutures in relation to sutures of preand postcingular plates (aÌ er Carty 1986). Fig. 3f. Sulcal plates (aÌ er Boltovskoy 1975). Peridinium gatunense Nygaard is spherical with no dorsoventral compression, has wide cingular lists and a small ¬ rst apical plate. Peridinium raciborskii Wołoszynska is large (70-80μm), 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 1ʹ plate (Figs. 5a-c, 6, 8). Antapical plates are about equal in size (Fig. 5d). ̈ e six cingular plates are not neatly aligned with preor postcingular plates except for the mid dorsal alignment of all three (Fig. 5e). Sulcal plates di3 er individually from their counterparts in P. cinctum, especially the Sd in P. umbonatum which forms a distinctive È ap over the È agellar pore (Figs. 5f, 6). On the dorsal surface the two apical intercalary plates, and the 3ʹ and 4ʹʹ plates have a plastic relationship, conjunctum when the 3ʹ and 4ʹʹ 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 3ʹ and OHIO JOURNAL OF SCIENCE 105 S. CARTY Figures 4 and 5. Line drawings. Fig. 4 Original drawing from Stein 1883. Fig. 5a. Ventral view. Fig. 5b. Dorsal view, 3ʹ and 4ʹʹ conjunctum. Fig. 5c. Apical view with plates identi¬ ed, 3ʹ and 4ʹʹ conjunctum. Fig. 5d. Antapical view. Fig. 5e. Cingular plates with sutures in relation to sutures of preand postcingular plates (aÌ er Carty 1986). Fig 5f. Sulcal plates, note Sd forming È ap over È agellar pore (FP) (aÌ er Carty 1986). Fig 5g. Plates 3ʹ and 4ʹʹ contactum Fig 5h. Plates 3ʹ and 4ʹʹ remotum (aÌ er Lefèvre 1932). 4ʹʹ are separated (Fig. 5h)(Lefèvre 1932). Lefèvre (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 (Elbrächter and Meyer 2001). Plate È uidity is characteristic of some taxa like the species in the Umbonatum Group, ompsodinium (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 ornamentation, cells are small (12-20μm diameter), and forms/varieties oÌ en have spines (Table 1). Species within the Umbonatum group are distinguished by overall shape, presence of spines, and plate sizes and positions. Popovský and P¬ ester (1986, 1990) synonomized many species with P. umbonatum (retaining P. morzinense and P. a icanum) as varieties (var. centenniale, var. de¦ andrei, 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. Sexual reproduction has been investigated in P. cinctum (P¬ ester 1975) and P. inconspicuum in the Umbonatum Group (P¬ ester 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 (P¬ ester 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). ̈ ese two 106 VOL. 108 UMBONATUM GROUP OF PERIDINIUM studies add credence to the separation of the Umbonatum group from Peridinium. Parvodinium Carty genus novum Dino¦ agellatum aquae dulcis, ovatae ad quinqueangulatus, theca tenue, ordinatione tabulari Po, 4ʹ, 2a, 7ʹʹ, C6, S5, 5ʹʹʹ, 2ʹʹʹʹ, chromatophoris aureus, epitheca hypothcamsuperantia, cingulum latum. Freshwater dinoÈ agellate, small, ovoid to pentagonal cell, plates thin, plate pattern: apical pore, pore plate, canal plate, 4ʹ, 2a, 7ʹʹ, C6, S5, 5ʹʹʹ, 2ʹʹʹʹ, 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; 3ʹ and 4ʹʹ plates may be in conjunctum, contactum or remotum positions. Type species: Parvodinium umbonatum (Stein) Carty comb. nov. Etymology: parvo (L) small, din whirling Parvodinium a icanum (Lemmermann) Carty comb. nov. Basionym: Peridinium a icanum Lemmermann ex West 1907 J. Linn. Soc. Bot. 38:188 Pl 9 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 ¬ g 14. Parvodinium de¦ andrei (Lefèvre) Carty comb. nov. Basionym: Peridinium de¦ andrei Lefèvre 1927. Bull. Mus. Hist. Nat. Paris 33:121 Parvodinium goslaviense (Wołoszyńska) Carty comb. nov. Basionym: Peridinium goslaviense Wołoszyńska 1916. Bull. Acad. Sci. Cracovie Sér. B. p267 Taf 10, Fig 18-24. Parvodinium inconspicuum (Lemmermann) Carty comb. nov. Basionym: Peridinium inconspicuum Lemmermann 1899. Abh. Nat. ver. Breman, XVI p350 Figures 6-8. Scanning electron micrographs of P. umbonatum. Fig. 6. Ventral view, plates numbered. Fig. 7. Dorsal view. Fig. 8. Apical view, cp = canal plate. Table 1 Dia erences between Peridinium cinctum and Parvodinium umbonatum Feature Peridinium Parvodinium