Diatom Research (2006), Volume 21 (2), 269-280

AN EMENDED DESCRIPTION OF DECUSSATA (PATRICK)

PROTOPLAST ORGANIZATION AND DETAILED VALVE AND CINGULUM ULTRASTRUCTURE

LANGE-BERTALOT & METZELTIN THAT INCLUDES

Mark B. Edlund St. Croix Watershed Research Station, Science Museum of Minnesota,

16910 152ndSt. N., Marine on St. Croix, MN55047, U.S.A.

Lynn A. Brant Department of Earth Science, University of Northern Iowa

Cedar Falls, IA 50614, U.S.A.

Zlatko Levkov & Teofil Nakov Institute of Biology, Faculty of Natural Sciences, Gazi Baba bb,

P. 0. Box 162, 1000 Skopje, Republic of Macedonia

The subgenus DECUSSATA R.M. Patrick was recently elevated to generic status as Decussata (R.M. Patrick) H. Lange-Bertalot & Metzeltin in Lange-Bertalot (2000. Iconographica Diatomologica, 9, 670-673) to accommodate Navicula placenta Ehrenberg and its allies. The description of Decussata is based on characteristics of the valve: solitary cells, flat, broadly elliptic valves with various ends, and areolae with circular foramina arranged in regular quincunx patterns crossing at 60"-80". A collection from Cedar Hills Sand Prairie in Black Hawk Co., Iowa (U.S.A.), had abundant live Decussata placenta (Ehrenberg) Lange Bertalot & Metzeltin in Lange-Bertalot, the generitype, and a collection from near Prava Reka, Macedonia, had numerous specimens of Decussata hexagona (Torka) Lange-Bertalot. These collections permitted a first observation of living Decussata and a detailed study of their valve and cingulum ultrastructure. Based on this material we place Decussata in the Order Mastogloiales and Family Mastogloiaceae, and provide an emended description of the genus to include details of valve ultrastructure including structure of the cingulum, areolae occluded by internal convex hymenes, and the protoplast characters of a central nucleus, two chloroplasts per cell, one toward each pole, H-shaped in girdle view, variably invaginated in valve view, with a pyrenoid in the plastid bridge.

INTRODUCTION

Early diatom workers recognized the systematic value of protoplast organization (Mereschkowsky 1901, Heinzerling 1908) and several genera were described using chloroplast morphology as supporting evidence (e.g. Mereschkowsky 1902, 1903). Much of this detailed cytological work later fell out of favor as mid-20th century diatomists focused their systematic efforts solely on frustule features. More recently, workers have again recognized the systematic and taxonomic significance of protoplast features and have used this evidence to support circumscription of new genera (e.g. Round et al. 1990), to resurrect older

Author to whom correspondence should be addressed, e-mail: mbedlund@smm.org 1

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genera (e.g. Cox 1987), and to support phylogenetic hypotheses (Kociolek & Stoermer 1988, Schmid 2001).

Decussata (R.M. Patrick) Lange-Bertalot (2000) was recently transferred to genus level from the subgenus Decussata Patrick ( 1959) to accommodate Navicula placenta Ehrenberg and its allies (Lange-Bertalot 2000). Patrick (1959) proposed the subgenus DECUSSATA based on Grunowk (1860) naviculoid Gruppe Decussatae, but Patrick did not base her subgenus on a species included in Grunow's Gruppe. The generitype, Decussata placenta (Ehrenberg) Lange Bertalot & Metzeltin in Lange-Bertalot (2000), is widely reported, but often as rare (Patrick & Reimer 1966, Krammer & Lange-Bertalot 1986, Lange-Bertalot 2001). Decussata was described solely on valve characters and is characterized by solitary cells, flat and broadly elliptic valves with various end shapes, and areolae with circular foramina arranged in a regular decussate or quincunx pattern with striae crossing at 60"-80" (Figs 1-15). As currently understood, the genus Decussata is made up of three taxa: D. placenta, D. placenta var. obtusa (Meister) Lange-Bertalot, and D. hexagona (Torka) Lange-Bertalot. In the description of the genus it is noted that "the three taxa.. .are altogether rare and scarcely observed in their habitats as living cells.. ." (Lange-Bertalot 2000). Furthermore, Patrick (1959) did not report on the living condition in her description of the subgenus DECUSSATA. Herein, we provide a first description of protoplast organization based on examination of live material and further detail on valve and cingulum structure of Decussata.

MATERIAL AND METHODS

Cedar Hills Sand Prairie in Black Hawk County, Iowa, U.S.A., is a 35-ha preserve of which about 14 ha are native prairie. A seep of imperceptible flow consisting of saturated ground with footstep-sized pockets of standing water 0-10 cm deep occurs along the north edge of an east-west slough in the native portion of the prairie (42°35'38.1"N, 92'32'59.7"W). The seep is characterized by slightly acidic (pH 6.04.5) and low conductivity (58-87 pS) water; this is unusual for surface waters in Iowa. The prairie in general and the seep in particular supports a soft-water diatom flora (Dodd 198 1). Decussata placenta is always found in the seep. One of us (L.A.B.) has collected this species from the seep since 1996. Decussata placenta is common (6% of all diatoms in one count) in all six of the mounted collections examined for this study, which were obtained between 1996 and 2002 in the months of May, July, September, and October. A collection made 04 July 2004 from this seep contained abundant live D. placenta allowing the observation of protoplast organization in this taxon. Several other collections (Isle Royale, Michigan; Jargalant Gol, Mongolia, Mammoth Cave, Kentucky) containing D. placenta in the personal collection of MBE were also consulted.

Decussata hexagona was collected on 26 September 2004 from a small peat-bog near Prava Reka, Macedonia, at 1420 m a.s.1. (40"59'44"N, 21'47'16"E). The peat-bog is characterized by a neutral pH of 7.2 and low conductivity (75 pS cm-'). Most of the peat-bogs in the Nidze Mountains are neutral to slightly alkaline due to calcareous geology, and support mainly neutrophilous and alkaliphilous diatoms including Achnanthes sensu lato, Navicula, and Placoneis. In this collection, D. hexagona was at less than 1% relative abundance. Cleaned material of D. hexagona was studied from two other localities in Macedonia: a small peat bog about 1 m2 in the Shara Mountains (Levkov et al. 2001) and in an aerophytic bryophyte community growing in small ponds almost without water and with a large quantity of detritus located in the Nidze Mountains (Levkov et al. 2005).

Live cells and cleaned material were studied under oil immersion brightfield, phase contrast, and differential interference optics. Peroxide-cleaned material was also studied in a Zeiss DSM 960A operating at 20 kV after coating with 20 nm Au-Pd.

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Figs 1-7. Decussata placenta, cleaned valves, brightfield light microscopy, scale bar = 10 pm (in Fig. 1). Figs 1 4 . Size series from Cedar Hills Sand Prairie, Black Hawk County, Iowa, USA. Fig. 5. Isle Royale, Lake LeSalle, Michigan, USA (MBE 1433). Fig. 6. Mammoth Cave National Park, Kentucky, USA (MBE 1076). Fig. 7. Mongolia, Hovsgol National Park, Jargalant Gol, backwater sediments (M498) Figs 8-15. Decussata hexagona, from peat-bog near Prava Reka, Macedonia, cleaned valves, DIC light microscopy, scale bar = 10 pm (in Fig. 8). Fig. 16. Iconotype of Navicula (Ceratoneis) decussata Ehrenberg (1854, P1. 33/12, Fig. 23) from Columbia River, Oregon, USA. Fig. 17. Navicula placenta Ehrenberg as illustrated in Schmidt (1874-1959, Tfl. 188 Fig. 33), sample from Singapore. Fig. 18. Iconotype of N. placenta var. oblongu Meister (1935, Tfl. 13, Fig. 99) from the Saigon-River, Cochinchina. Fig. 19. Iconotype of Navicula placenta var. minor Krasske (1 923). Fig. 20. Iconotype of Navicula placenta var. parallela Krasske (1925). Figs 21-22. Icontypes of Navicula hexagona Torka ( 1 933).

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RESULTS

From our observations we offer an emended description of the genus Decussata that includes protoplast characters and details of valve and cingulum ultrastructure. Our observations supplement earlier observations of valve ultrastructure by Lange-Bertalot (0. placenta; 2000,2001) and Stancheva & Temniskova (0. hexugona, 2006).

Decussata (R.M. Patrick) H. Lange-Bertalot & D. Metzeltin emend M.B. Edlund,

Generitype: Decussuta placenta (Ehrenberg) Lange Bertalot & Metzeltin in Lange-Bertalot L.A. Brant, Z. Levkov & T. Nakov

(2000) Naviculaplacenta Ehrenberg (1854), pl. 33, Figs 12/23.

Description:

Frustule Cells living solitary (Figs 1-15, 23-40). Valves broadly elliptic to linear tapering to the

obtusely cuneate to broadly rounded or rostrate ends (Figs 1-15, 18). In girdle view narrowly rectangular (Fig. 25). Valve face flat, valve mantle narrow and perpendicular to valve face (Figs 41, 53). On valve exterior, central area circular to oval, axial area narrow, raphe filiform with slight sinuous discontinuity immediately adjacent to the terminal deflection, and central raphe endings expanded as croziers deflected to the same side of the valve on valve exterior (Figs 1-15, 18,41,43, 53, 57). External terminal raphe fissures asymmetrically overlapped by a silica fold, deflected to opposite sides of the valve (Figs 41, 45-46, 53-54). Internal raphe fissure straight between thickened internal ribs, central ends each with a small linear thickening at central nodule, terminal ends with expanded helictoglossae (Figs 42, 44, 47-48, 55-56, 58). Areolae with circular foramina on valve exterior and arranged in a regular quincunx pattern to produce three systems of striae which cross each other at angles of 60"-80" (Figs 1-15, 41, 43, 53-54). Each areola occluded internally by a circular convex hymene (Figs 44, 58). Striae continuous from valve face onto mantle and striae pattern similar on internal surface of valve (Figs 45-46, 53-54,56). Oblique costae of the quincunx system at least in the central part of the valve with moderately higher internal relief than the transapical costae (Figs 44, 58). Cingulum of 3-4 open bands (Fig. 49); each band with two rows of areolae (Figs 5 1-52), valvocopulae with reflexed advalvar margin (Fig. 52).

Protoplast Nucleus located centrally within a cytoplasmic bridge between the central nodules

(Figs 23-24, 26-40). Each cell with two chloroplasts. Chloroplasts are separated by the transapical cytoplasmic bridge with one chloroplast located toward each cell pole (Figs 23- 40). Plastids are H-shaped in girdle view (Fig. 25) and transapical cross-section with the four arms of the plastid extending along the valve faces in the valvar plane; two arms extend along each valve face reaching the cingulum region (Fig. 25) where secondary folding may be present (Figs 23-40). The plastids.are also invaginated along the apical axis to create a central plastid isthmus that contains a refractile linear to cuboidal body that is likely the pyrenoid (Figs 23-24,2640). Secondary transapical invaginations of the plastid arms were also seen in some cells (Figs 35-37). No libroplasts noted.

As currently circumscribed, the genus Decussata comprises three taxa: D. placenta, D . placenta var. obtusa, and D. hexagona. Decussata placenta was described by Ehrenberg (1854) from the "Brakischer Tripe1 vom Columbia-River'' in Oregon, U.S.A. (Fig. 16) and is reported rare but widespread throughout the northern hemisphere (e.g. Cleve-Euler 1955, Patrick & Reimer 1966, Camburn et al. 1978, Dodd 1981, Foged 1981, Hartley et al. 1996,

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Figs 23-37. Live cells of Decussata placenta showing variability of protoplast structure, Cedar Hills Sand Prairie, Black Hawk County, Iowa, USA, light microscopy, scale bar = 10 pm (in Fig. 23). Figs 23-24. Brightfield optical series of live cell in valve view, high and mid focus. Fig. 25. Girdle view, brightfield, showing two arms of chloroplasts positioned along the valve faces. Figs 26-28. Phase contrast optical series, valve view, high, mid and low focus. Figs 29-31. Brightfield optical series, valve view, high, mid and low focus. Figs 32-34. Brightfield optical series, valve view, high, mid and low focus. Figs 35-37. Brightfield optical series, valve view, high, mid and low focus. Figs 3840. Live cell of Decussata hexagona, peat-bog near Prava Reka, Macedonia. Brightfield optical series in valve view, high, mid, and low focus, scale bar = 10 pm (in Fig. 40).

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Figs 41-48. Decussata placenta, SEM. Fig. 41. External view of frustule. Scale bar = 10 pm. Fig. 42. Internal view of valve. Scale bar = 10 pm. Fig. 43. External view of oval central area with unilaterally deflected crozier-shaped proximal raphe ends. Scale bar = 2 pm. Fig. 44. Internal view of central area with linear thickenings of proximal raphe ends and areolae occluded internally with circular hymenes. Scale bar = 2 pm. Figs 45-46. External terminal raphe endings deflect in opposite directions and are covered by a siliceous flap. Scale bars = 2 pm. Figs 47-48. Internal view of moderately expanded helictoglossa at terminal raphe ends and filiform raphe between two thick internal longitudinal ribs. Scale bars = 1 pm.

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Figs 49-52. Decussata placenta, SEM, cingulum structure. Fig. 49. External view of frustule end with 3 4 open girdle bands. Scale bar = 2 pm. Fig. 50. Advalvar margin of valvocopula has a reflexed flange that interlocks with valve margin. Scale bar = 2 pm. Figs 51-52. Opposite ends of open girdle band ornamented with two rows of areolae on the pars interior. Scale bars = 4 pm.

Stoermer et al. 1999, Johansen et al. 2004). The habitat preference of D. placenta is oligotrophic lakes, springs, moss communities, and aerophilic collections, although several authors report this taxon from brackish sites (Schmidt in Schmidt et al. 18741959, Hartley et al. 1996) including the type locality (Ehrenberg 1854). Specimens examined in this study (Figs 1-7) correspond well to published descriptions of this species: elliptical valves with apiculate-rostrate ends, length 3041(45) pm, breadth 13-16(20) pm, striae 19.5-25/10 pm, finer at the ends, areolae 20-22/10 pm. Collections from Iowa had smaller specimens than most reports. Decussata placenta var. obtusa has been reported only from its type locality in Saigon (Fig. 18). Schmidt's (18741959; Tfl 188, Fig. 33) depiction of N. placenta (Fig. 17) from Singapore may also correspond to this taxon. This taxon is in need of detailed SEM analysis. Decussata hexagona was originally described by Torka (Figs 21-22; 1933) from Kreise Neustadt (Oberschlesien, Germany). Two taxa earlier described by Krasske as varieties of N. placenta, N. placenta var. minor Krasske (Fig. 19; Krasske 1923) and N. placenta var. parallela Krasske (Fig. 20; Krasske 1925), are considered synonymous with Torka's taxon by Lange-Bertalot (2000). Analysis of D. hexagona from Macedonia agrees with this interpretation; the shape variation and size series encompasses the taxon identified by Torka and Krasske's forms. Decussata hexagonu is limited in its distribution to Europe and is uncommonly reported from bryophyte and peat collections (Torka 1933, Levkov et al. 2001, 2005, Stancheva & Temniskova 2006). Macedonian material corresponds well to published accounts: length 26-53 pm, breadth 10-12.7 pm, transverse striae 22-24/10 pm, oblique striae 16-19/10 pm, areolae 18-19/10 pm. Some Macedonian specimens are larger than previously reported for this taxon.

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Figs 53-58. Decussata hexagona, SEM. Fig. 53. External view of frustule. Scale bar = 5 pm. Fig. 54. External terminal raphe end covered by a siliceous flap. Scale bar = 2 pm. Fig. 55. Internal view of moderately expanded helictoglossa at terminal raphe ends and filiform raphe between two thick internal longitudinal ribs. Scale bar = 2 pm. Fig. 56. Internal view of valve. Scale bar = 10 pm. Fig. 57. External view of transapically oval central area with unilaterally deflected crozier-shaped proximal raphe ends. Scale bar = 2 pm. Fig. 58. Internal view of central area with linear thickenings of proximal raphe ends and areolae occluded internally with circular hymenes. Scale bar = 2 pm.

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Two other forms of Navicula placenta have been described that bear little resemblance to Decussata: N. placenta f. curta (Skvortzov) Skvortzov (1929, 1946) and N. placenta f. nipponica Skvortzov (1936). The former taxon comprises three forms earlier described by Skvortzov (1 929): N. peregrina var. minuta Skvortzov, its f. curta Skvortzov, and N. gastrum var. limnetica Skvortzov. All of these taxa are illustrated with lineolate striae that are radiate and bear little resemblance to the Decussata-type striae. Navicula placenta f. nipponica may be a typographical error. Although illustrated with that name, the text description (Skvortzov 1936: 38) refers to this taxon as N . placentula f. nipponica Skvortzov and the illustrated specimen appears more closely allied with N. (Placoneis) placentula (Ehrenberg) Kutzing.

DISCUSSION

Patrick (1 959) erected the subgenus DECUSSATA based on Grunow’s (1 860) Gruppe Decussatae. Grunow (1 860) segregated this “Gruppe” based on multiple striae patterns and included in it the following species: Navicula sphaerophora Kutzing, N. tuscula Ehrenberg, N. rostrata Ehrenberg?, N. costata Kutzing, N. tumens W. Smith, N. decussata Ehrenberg in Kutzing, and N. pannonica Grunow. Patrick (1959) typified the subgenus DECUSSATA based on N. placenta, commenting that this common taxon served as a better type for the subgenus than the more rare N. decussata. In describing the subgenus DECUSSATA, Patrick (1959) used the term “subg. nov.” and attributed the name to Grunow (see also Patrick & Reimer 1966), but ironically Grunow (1 860) did not recognize N. placenta as a member of his Gruppe. As such, the proper authorship at the genus level should be Decussata (R.M. Patrick) Lange-Bertalot & Metzeltin emend Edlund et al.

Protoplast arrangement in Decussata placenta is classified as “group M ’ by Cox (1996) in her artificial taxonomic key: two chloroplasts per cell, one toward each pole, or H-shaped in girdle view with a pyrenoid in the plastid bridge. This arrangement is found in Aneumastus D.G. Mann & Stickle, Cavinula D.G. Mann, Mastogloia Thwaites in W. Smith, and some small Neidium Pfitzer species (Stoermer et al. 1964, Round et al. 1990, Cox 1996). Mereschkowsky (1 902-1 903) separated this arrangement within his “endochrome” Type I. Polyplacatae, Group I1 Tetraplacatae, which included the families Neidieae, Scoliotropidae, and Mastogloiae. In addition to chloroplast number and arrangement, pyrenoid location and structure have also been shown to have systematic value in the classification of diatoms (Schmid 2001). We were not able to unambiguously demonstrate the presence of the pyrenoid in the plastid isthmus or bridge (aside from a slight refractile signal in LM); however, Stoermer et al. (1964) documented the location and character of the pyrenoid in this chloroplast type in Mastogloia grevillei W. Smith using transmission electron microscopy.

Although Decussata was erected based solely on valve characters (Lange-Bertalot 2000), protoplast arrangement provides hrther clues as to the systematic placement of this taxon. Decussata is obviously not closely allied with Navicula sensu stricto with regard to either valve morphology or protoplast arrangement. Decussata has circular areolae occluded with internal hymenes compared to lineolate areolae occluded by internal hymenes in Navicula sensu stricto (Round et al. 1990). Decussata areolae also differ significantly from the complex areolae types found in Aneumastus, Mastogloia, and Neidium (Round et al. 1990). More importantly, the two H-shaped chloroplasts situated toward each pole in the cells of Decussata, differ significantly from the two plate-like girdle-appressed chloroplasts of Navicula sensu stricto.

We propose that Decussata is best accommodated within the Order Mastogloiales and Family Mastogloiaceae. Protoplast organization in Decussata is shared with other members of the Mastogloiaceae, namely Mastogloia and Aneumastus (Mereschkowsky 1902-1 903, Stoermer et al. 1964, Round et al. 1990, Cox 1996). Mastogloia is a large genus with much

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character variation in frustule ultrastructure (Paddock & Kemp 1990); however, several Mastogloia share characters with Decussata. Mastogloia dissimilis Hustedt, M, lata Hustedt, M. decussata Grunow have areolae arranged in a quincunx pattern to produce transverse and oblique striae patterns. Internal terminal raphe endings are variable in Mastogloia; however, Decussata shares similar construction with those in M. stephensiana Yohn & Gibson and M. cyclops Voight (Paddock & Kemp 1990). External terminal raphe ends in Decussata are characterized by opposite deflection and coverage by a siliceous flap. In contrast, terminal raphe ends appear unilaterally deflected in many Mastogloia and Aneumastus, but M. decussata does have a siliceous terminal raphe flap (Paddock & Kemp 1990). Although many Mastogloia and Aneumastus species have sinuous external raphe slits, some taxa have filiform slits reminiscent of Decussata, including M. pusilla Grunow (Paddock & Kemp 1990). There is a slight sinuous discontinuity just before the terminal raphe deflection in Decussata. The reflexed advalvar edge of the valvocopula that couples the band to the valve in Decussata is shared with Mastogloia (Stoermer et al. 1964) and Aneumastus (Round et al. 1990). Among the characters that separate Decussata within the Mastogloiaceae are the simple areolae occluded by internal hymenes, linear thickening of the internal proximal raphe ends, and no chambering on the valvocopulae.

Round & Sims (1981) and Mann (1999) noted that many diatom genera are limited in their distribution by the strong ecological and physiological gradient that exist between marine and freshwater habitats. Round & Sims (1981) further noted that many of the genera recognized at that time (1981), which had species inhabiting both marine and freshwater environments, represented unnatural taxonomic groups. This observation led, in part, to many of the genera that were described, segregated, or resurrected in Round et al. (1 990). However, even after the generic revisions of the 1990~-2000s, a few genera are still found with representatives in both freshwater and marine habitats. Surirella, Campylodiscus, Navicula, Achnanthes, Diploneis, and Amphora come to mind, but of particular interest are the members of the family Mastogloiaceae. Mastogloia is more diverse in marine habitats, but a rich flora inhabits alkaline and inland saline habitats. The genus Decussata may follow this pattern. Decussata placenta var. obtusa as well as two other naviculoid diatoms with quincunx areolae arrangement, Navicula quincunx Cleve and N. placentiformis Hustedt (Hustedt 1962), are reported from brackish or marine habitats. All three of these taxa beg to be further studied in SEM and living condition to determine if they belong in Decussata. If they are found to belong to Decussata, this genus will be one of the few that is well-diagnosed and shares taxa in both marine and freshwater habitats.

ACKNOWLEDGEMENTS

Thanks are extended to Iowa Lakeside Laboratory, site of the annual summer diatom course since 1963, for providing facilities, Jeff Thole and Charles Conway for assistance and use of the SEM facilites at the Keck Laboratory, Macalaster College, Steve Main, for assistance and use of the SEM at Wartburg College, and Rosalina Stancheva, for access to her manuscript on ultrastructure of Decussata hexagona. This project was supported by a Summer Fellowship to Lynn Brant, the Department of Earth Science, and the College of Natural Sciences at the University of Northern Iowa. This material is based partly upon work supported by the National Science Foundation (NSF) under grant DEB-03 16503 to MBE. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the NSF.

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