HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

(American Journal of Botany. 2009;96:487-497.) doi: 10.3732/ajb.0800307 © 2009 Botanical Society of America, Inc.

What's this?

This Article Abstract Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Wolfe, A. P. Articles by Siver, P. A. Search for Related Content PubMed Articles by Wolfe, A. P. Articles by Siver, P. A. Agricola Articles by Wolfe, A. P. Articles by Siver, P. A. Social Bookmarking                            What's this?

Three extant genera of freshwater thalassiosiroid diatoms from Middle Eocene sediments in northern Canada¹

² Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB T6G 2E3, Canada ³ Botany Department, Connecticut College, New London, Connecticut 06320 USA

Received for publication 11 September 2007. Accepted for publication 21 October 2008.

ABSTRACT

The evolutionary history of diatoms is only constrained partially by the fossil record. The timing of several key events, such as initial colonization of freshwater habitats by marine taxa, remains poorly resolved. Numerous specimens of the genera Cyclotella, Discostella, and Puncticulata (Ochrophyta: Thalassiosirales) have been recovered in Middle Eocene lacustrine sediments from the Giraffe Pipe locality in the Northwest Territories, Canada. These diatoms extend the fossil record of the family Stephanodiscaceae to at least 40 million years before present (Ma) and thus provide a new evolutionary milepost for the thalassiosiroid diatoms, an important clade of centric diatoms with global representation in both marine and freshwater environments. The quality of the fossil material enables detailed investigations of areolae, fultoportulae, and rimoportulae, revealing direct morphological affinities with a number of extant taxa. These observations extend the antiquity of several characters of phylogenetic importance within the thalassiosiroid diatoms, including the fultoportula, and imply that the entire lineage is considerably older than prior constraints from the fossil record, as suggested independently by several recent molecular phylogenies.

Key Words: Cyclotella • Discostella • Eocene • evolution • fossil diatoms • fultoportula • morphology • Puncticulata • Thalassiosirales

Diatoms are a highly successful clade of microscopic photoautotrophs, accounting for approximately 20% of global photosynthesis (Falkowski and Raven, 1997). However, the evolutionary history of the diatoms is poorly understood relative to other major phytoplankton groups, ultimately limiting the extent to which hypotheses concerning their rise to ecological prominence can be evaluated (Falkowski et al., 2004). Poor concordance between molecular and paleontological estimates of major events in diatom evolution places a premium on fossil localities with exceptional preservation and adequate geochronology.

The order Thalassiosirales Glezer and Makarova contains about 40 validly published genera of living and fossil diatoms that are distributed globally in freshwater and marine environments (Table 1). These diatoms present an impressive array of morphological characters, including fultoportulae (strutted processes), rimoportulae (labiate processes), and in some taxa, loculate areolae with internal cribrae. Valve-face areolae frequently form striae with either linear or radial arrangements. In several genera, areolae are organized as distinct fascicles with or without internal radial costae on the interstriae. Despite considerable morphological and ecological diversity, the Thalassiosirales form a robust natural group in all recent molecular phylogenies, with the nonfultoportulate Lithodesmiales Round and Crawford as the sister clade (Fox and Sörhannus, 2003; Sörhannus, 2004; Kaczmarska et al., 2006; Sims et al., 2006). Within the thalassiosiroid lineage, the families Thalassiosiraceae Glezer and Makarova and Stephanodiscaceae Lebour are the most common and diversified (Table 1). Thalassiosira Cleve is the most speciose genus in the order, with about 180 and 12 marine and fresh-water species, respectively (Round et al., 1990). This genus includes the first diatom for which the entire genome was sequenced, T. pseudonana Cleve, yielding a relatively compact genome (34.5 mega base pairs) that nonetheless elucidates the complexity of diatom origins (Armbrust et al., 2004). Furthermore, the culturing of Thalassiosira has been central to major developments in algal toxicology, physiology, and biochemistry (e.g., Rueter and Morel, 1981; Harrison and Morel, 1986; Roberts et al., 2007). Marine representatives of Thalassiosira appear closely related to several freshwater genera of the family Stephanodiscaceae, the so-called cyclostephanoid group that includes Cyclostephanos Round, Cyclotella Kützing ex de Brébisson, Discostella Houk and Klee, Puncticulata Håkansson, and Stephanodiscus Ehrenberg. It has been proposed that these genera originated from multiple events of freshwater colonization by marine thalassiosiroid taxa (Kaczmarska et al., 2006; Sims et al., 2006). Additional molecular approaches involving both nuclear and chloroplast gene sequences confirm elegantly this polyphyletic model of diversification into freshwater habitats (Alverson, 2007; Alverson et al., 2007). However, the timing of these hypothesized evolutionary radiations remains poorly constrained. Continued interrogation of the fossil record is therefore necessary to furnish mileposts for various evolutionary events among the thalassiosiroid diatoms.

MATERIALS AND METHODS

Study site
The Giraffe Pipe locality (64°44'N, 109°45'W) is a kimberlite diatreme that has been infilled by a sequence of Middle Eocene lacustrine and paludal sediments and subsequently back-filled by Neogene glacigenic sediments (Fig. 1). The Giraffe Pipe is one of many kimberlites in the Lac de Gras field, most of which have Cretaceous or Paleogene emplacement ages (Heaman et al., 2004). A 165-m drill core collared at 47° was raised by BHP Billiton Diamonds in 1999 (core BHP 99–01) to assess the diamond potential of kimberlite underlying the crater fill. Core BHP 99–01 contains 113.1 m of stratified organic sediment of Middle Eocene age, including 44.8 m of peaty material underlain by 68.3 m of lacustrine mudstone. Conversion of these core depths to their vertical equivalents implies stratigraphic thicknesses of 32.7 m for the peat and 51.1 m for lake sediments (Fig. 1). Two air-fall tephra beds occur at the transition between lacustrine and paludal sedimentation, which marks the final infilling of the maar and incipient colonization by a forest composed dominantly of Metasequoia Miki ex Hu and Cheng (Cupressaceae).

View larger version (43K): [in this window] [in a new window]   Fig. 1. (A) Location of the Giraffe pipe fossil locality, (B) schematic stratigraphy of posteruptive sediments in the kimberlite diatreme, and (C) detailed lithostratigraphy and chronology of core 99–01. The interval of core considered in the current study is in boldface in (C), whereas stars indicate the depths illustrated in Fig. 2.

View larger version (125K): [in this window] [in a new window]   Fig. 2. Examples of Giraffe Pipe lacustrine sediments. The core contains mudstone that ranges from (A) massive to (B) fissile. In many sections, (C) macroscopic opal-A nodules are evident as subparallel partings. (D) Petrographic thin sections indicate that organic-rich mudstones are frequently finely laminated. Dark laminae comprise amorphous organic matter and chrysophyte cysts, whereas light laminae are composed of chrysophyte cysts and occasional diatom valves. (E) Surfaces of individual bedding planes often reflect massive chrysophyte cyst deposition events. Intact diatoms, including the taxa reported here, can occur in association with these cyst beds in trace abundances. These images are centered on the following core depths: 116.1 m (A), 109.9 m (B), 149.7 m (C), 150.1 m (D), and 121.3 m (D), as indicated in Fig. 1C.

Sample preparation
Specimens were prepared for scanning electron microscopy (SEM) as follows. Small chips (200 mg) of mudstone were first oxidized with 30% H₂O₂ overnight to attack organic matter, and then centrifuged and rinsed several times with deionized water (reverse-osmosis filtration). Samples of cleaned slurry were air-dried onto heavy-duty aluminum foil, trimmed, and mounted to aluminum stubs with Apiezon wax. Additional examinations were made of unprepared material. In this case, fresh fractures perpendicular to bedding planes were mounted onto stubs with double-sided carbon tape, and ringed with silver paint. These stubs were sputter-coated with Au or Au-Pd mixtures, prior to examination with either a Leo 982 (University of Connecticut) or a JEOL-6301F (University of Alberta) field-emission SEM. For light microscopy (LM), both H₂O₂-digested slurries and untreated disaggregated mudstone (<125 µm fraction) were mounted in Naphrax and examined under oil immersion objectives.

RESULTS

Despite excellent and continuous preservation of biogenic silica in the lower lacustrine facies of the Giraffe pipe core, diatoms are relatively uncommon. Chrysophyte stomatocysts, scales, and bristles are by far the most abundant siliceous microfossils. Cysts often constitute discrete laminae, but are also abundant in the organic-rich sediment matrix (Fig. 2D, E). Siliceous sponge spicules and gemmoscleres (birotules), as well as euglyphid protozoan scales (testate amoebae), are also more abundant than diatoms. From the census of SEM observations, we estimate that diatoms represent 0.5–5.0% of total siliceous microfossils. The most common diatoms in this portion of the core are araphid pennate taxa, including Fragilaria Lyngbye, Fragilariforma (Ralfs) Williams and Round, Oxyneis Round, Staurosira (Ehrenberg) Williams and Round, and Staurosirella Williams and Round, which will be reported upon separately. However, in the course of intensive SEM efforts (i.e., >100 h), regular observations of several morphotypes of thalassiosiroid diatoms were made. These account for 10% of the total diatoms encountered, implying that between a few hundred and several thousand siliceous microfossils were examined for each thalassiosiroid diatom. Nonetheless, given the sheer richness in most samples, a typical SEM session would yield several observations of the thalassiosiroid forms.

Given the resemblance of these diatoms to modern taxa, serious concerns were raised concerning potential contamination, both in the laboratory and from stratigraphic remobilization. Multiple additional and independent preparations were conducted in our respective laboratories with previously unused glassware, revealing rare but consistent occurrences of these diatoms across a range of samples from the lower core. Subsequently, fragments of these diatoms, including broken valves and copulae, were observed embedded within the matrix of undigested freshly fractured surfaces, confirming that they are part of the primary sedimentary material. We found no evidence in any of our preparations for contamination by species that commonly co-occur with these diatoms in modern lakes, which we believe would have been conspicuous. The possibility that these microfossils were leaked from younger strata can also be discounted because the 30 m peat facies that overlies the lake sediments is devoid of diatoms and chrysophyte microfossils. Furthermore, material originating from the outer core surface was consistently excluded by sampling only freshly fractured surfaces well beneath the surface, hence obviating the possibility of contamination during drilling. Finally, high-magnification SEM shows that the surfaces of these diatoms are lightly but visibly etched, to an extent not predicted for modern contaminants. Fortunately, this degree of etching does not impede observations of fine structures. Through these efforts, we have convinced ourselves that the diatoms we report here are indeed of Middle Eocene age. If additional authentication is warranted, voucher material is available upon request from the authors.

Cyclotella Kützing ex de Brébisson 1838 (Figs. 3–10)
Specimens observed from Giraffe pipe sediments conform in every way to current concepts of the genus Cyclotella (Round et al., 1990; Håkansson, 2002). Accordingly, Giraffe pipe Cyclotella have an undulating central area and robust radial costae (Figs. 3–5). Valve margin fultoportulae occur primarily adjacent to every fourth stria (Fig. 6), or occasionally every fifth or sixth (Fig. 8). Valve-face fultoportulae are clustered asymmetrically, opposite to both the prominent convex undulation (Figs. 3–7) and the single sessile rimoportula (Figs. 9–10). Valve-face fultoportulae generally have two satellite pores, although most specimens also possess a single fultoportula bearing three satellite pores (Fig. 7).

View larger version (180K): [in this window] [in a new window]   Figs. 3–10. Diatoms from the Giraffe pipe locality identified as Cyclotella. 3–5. Internal views of whole valves reveal the asymmetric disposition of valve-face fultoportulae opposite to the convex undulation of the central area and the single rimoportula, much as in the extant species C. michiganiana. 6–10. Magnifications of the areas outlined by white boxes reveals (Figs. 6, 8) marginal fultoportulae with two satellite pores, (Fig. 7) a single valve-face fultoportula with three satellite pores, and (Figs. 9–10) the single sessile rimoportula. Abbreviations: rp = rimoportula, mft = marginal fultoportula, and vfft = valve-face fultoportula. Scale bars are 10 µm for Figs. 3–5 and 1 µm for Figs. 5–10.

Discostella Houk and Klee 2004 (Figs. 11–22, 29)
A second group of thalassiosiroid diatoms observed in Giraffe pipe sediments is characterized by the stellate organization of the central area. Valves have a convex or concave central area, frequently with a colliculate external morphology (Fig. 11). Stellate alveoli are occluded by cribrae (Figs. 12–14), but in some cases do not fully perforate the valve face, resulting in depressions that express variably the stellate pattern (Figs. 17, 20, 22). Marginal fultoportulae have two satellite pores and are situated between costae, adjacent to every second to fourth stria (Figs. 15–21). A simple single rimoportula also occurs on the valve mantle (Figs. 18–21), but neither rimportulae nor fultoportulae are present on the valve face. All these features are entirely consistent with the diagnosis of Discostella by Houk and Klee (2004).

View larger version (184K): [in this window] [in a new window]   Figs. 11–22. Discostella from the Giraffe pipe material. Valves have either a convex central area with colliculate external morphology (Fig. 11) or are concave (Fig. 22). Internally, a stellate organization of alveolar openings with cribrate occlusions is present in some (Figs. 12–16), but not all (Figs. 17–22) specimens. White boxes indicate areas magnified in successive images. Abbreviations are as in the previous images. Scale bars are 5 µm for Figs. 11, 12, 14, 17, 20, and 22; 1 µm for Figs. 13, 15–16, and 18; and 0.5 µm for Figs. 19 and 21.

View larger version (126K): [in this window] [in a new window]   Figs. 29–34. Paired comparisons of Middle Eocene and modern Discostella and Puncticulata in LM. The upper row (Figs. 29–31) includes specimens from the Giraffe locality, whereas the lower row (Figs. 32–34) is from Ashumet Lake, Mashpee, Massachusetts, USA. (41.63°N, 70.54°W), and identified as D. stelligera (Fig. 32) and P. radiosa (Fig. 33–34). The Puncticulata pairs in each row are the same specimens viewed in different focal planes. Scale bars = 5 µm.

View larger version (158K): [in this window] [in a new window]   Figs. 23–28. Middle Eocene and modern specimens of Puncticulata. Internal view of a complete valve from the Giraffe pipe material (Fig. 23), showing the distribution of areolae, fultoportulae, and rimorportulae. The white boxes outline areas shown in high magnification (Figs. 24, 26). Note the presence of valve-face fultoportulae with both two and three satellite pores (Fig. 24). Oblique external view of another specimen from the Giraffe pipe, illustrating the concave central area and external openings of marginal fultoportulae (Fig. 23). Holocene specimens of P. radiosa from the Kangerlussuaq region of west Greenland (Lake SS32, 66.97°N, 49.8°W) are shown for comparison (Figs. 27, 28). Areolae with internally domed cribrae are abbreviated ar; other abbreviations are as in the previous images. Scale bars are 5 µm for Figs. 23, 25, and 27; 1 µm for Figs. 24 and 26, and 2 µm for Fig. 28.

DISCUSSION

The documentation of Middle Eocene freshwater thalassiosiroid diatoms with morphological affinities to modern taxa has numerous implications for the evolution of the lineage. The emergence of these diatoms in lakes of western North American had been hitherto assigned to the Middle and Late Miocene (Cylotella sensu lato followed by Mesodictyon Theriot and Bradbury), with further speciation during the Pliocene as Stephanodiscus and Cyclostephanos evolved (Krebs et al., 1987). These authors stated (p. 506) that they "are confident, however, that the general outline of lacustrine diatom biochronology presented herein will remain intact." While their biostratigraphic scheme has endured with respect to Mesodictyon, which appears restricted to the Late Miocene globally (Fourtanier et al., 1993; Khursevich, 2006), it is now concluded that the cyclostephanoid genera Cyclotella, Discostella, and Puncticulata had evolved by the Middle Eocene, in the order of 20 million years prior to previous estimates.

Central to arguments concerning thalassiosiroid evolution is the emergence of the fultoportula, which, while representing the defining character of the order Thalassiosirales, mandates both excellent preservation and the use of SEM to document satisfactorily. As the locus of β-chitin thread synthesis (Herth, 1978), the fultoportula is a synapomorphic trait for the thalassiosiroid lineage, to which this secondary metabolism appears unique. Threads produced by valve-face fultoportulae link adjacent cells into filamentous colonies, whereas those emerging from valve margin fultoportulae appear involved in cell buoyancy regulation (Walsby and Xypolyta, 1977). The oldest diatoms with fultoportulae unambiguously homologous to those of modern thalassiosiroids had recently been assigned to Poloniasira Kaczmarska and Ehrman, from the Late Oligocene (31 Ma) of Poland (Kaczmarska and Ehrman, 2008). The current study suggests that both marginal and valve-face fultoportulae were already present in nonmarine diatoms by the Middle Eocene. Concerning the evolution of the fultoportula, Kaczmarska et al. (2006 , p. 132) conceded cautiously that "the sequence of events leading to its formation is not known either from the fossil record or ontogenetically." However, only the scenarios of fultoportula evolution from either the areola or the multistrutted process pass the suite of homology tests required to be retained as testable hypotheses (Theriot, 2008). The relationship between the fultoportula and the multistrutted process of Late Cretaceous and Paleogene Thalassiosiropsis has been suspected since the genus was erected (Hasle and Syvertsen, 1985), and the inclusion of Thalassiosiropsis in Table 1 reflects our conviction that homology can be postulated between the multistrutted process and the fultoportula. The architecture of fultoportulae in the Giraffe pipe specimens implies that their morphology is highly conserved over the last 40 million years in the documented genera. This narrows the stratigraphic window in which to search for key transitional morphotypes: sediments of Late Cretaceous to Middle Eocene age, but capturing both marine and freshwater environments (Harwood et al., 2007). In a more general sense, the Giraffe pipe specimens indicate that the full complement of morphological characters that define modern thalassiosiroid diatoms had evolved much earlier than previously suspected. Two hypotheses can be invoked with respect to these observations.

First, the evolution of Thalassiosirales from extinct marine centric lineages of Cretaceous age may have occurred at an accelerated tempo. This possibility may be explored through analyses of three of the Early Cretaceous genera erected by Gersonde and Harwood (1990) , namely Gladiopsis, Praethalassiosiropsis, and Rhynchopyxis. If any of the features that characterize these genera, including the central annular, perforate, or rhyncho-shaped processes, can be proven homologous to the fultoportulae of thalassiosiroid diatoms, one or more of these taxa may yet be confirmed as the ancestral stock. Support exists for the potential of rapid speciation within the Thalassiosirales, as implied by a wealth of molecular (Kooistra and Medlin, 1996; Armbrust and Galindo, 2001) and stratigraphic (Edlund et al., 2000; Khursevich, 2006; Theriot et al., 2006) evidence. The scenario of accelerated evolution during the Cretaceous is not only consistent with these and other elements of the diatom fossil record (Sinninghe Damsté et al., 2004), but also mirrored by the spermatophyte and pteridophyte lineages on land (Schneider et al., 2004). Possibly, accelerated diversification occurred broadly across autotrophic clades at this time, in response to unique but unspecified environmental cues. One caveat to this scenario is that the backbone of the thalassiosiroid tree is relatively well resolved (Kaczmarska et al., 2006; Alverson et al., 2007), which likely places an upper limit on potential rates of speciation within the group.

A second possibility is that the entire thalassiosiroid lineage is considerably older than currently established, and inferences concerning its history have been complicated by the incomplete nature of the fossil record (Theriot, 2008). This view is consistent with molecular clocks using small subunit rRNA and various constraints from the fossil record, which suggest that the order Thalassiosirales is considerably older than implied by the available fossil record (Kooistra and Medlin, 1996; Sörhannus, 2007). Of course, the two hypotheses presented are not mutually exclusive. Moreover, the observations from the current study allow only the second to be addressed, until a fuller range of Cretaceous diatoms, including putative freshwater forms (Chacón-Baca et al., 2002), can be appraised in full morphological detail using SEM.

We argue here that it is primarily the limiting quality of the diatom fossil record that has led to discrepant age estimates for the origin of phylogenetically important characters such as the fultoportula. In this regard, exceptional fossil localities with well-constrained ages, such as the Giraffe pipe locality for Middle Eocene lakes, gain considerable importance. For example, this site has already extended by millions of years the fossil records of eunotioid diatoms (Siver and Wolfe, 2007) and of scaled chrysophytes (Siver and Wolfe, 2005). From the simple perspective of the outstanding preservation witnessed in this material, the discovery of thalassiosiroid diatoms is perhaps less surprising, all the more since the vast majority of siliceous microfossils observed to date can be attributed to extant genera. It is not only the morphology of these organisms, but also their autecologies, that appear largely unchanged since the Middle Eocene. For example, the three cyclostephanoid diatom genera reported here commonly co-occur in the phytoplankton of modern oligotrophic to mesotrophic lakes (Kling and Håkansson, 1988; Siver et al., 2005), much as they apparently did in the Middle Eocene Giraffe lake ecosystem. From the integration of these observations, we share the view that the diatom fossil record is likely considerably older than presently known, in keeping with the fact that molecular clocks place the origin of diatoms at least 100 Ma before the earliest unambiguous fossils, but unlikely earlier than 266 Ma (Kooistra and Medlin, 1996; Sims et al., 2006). As for the thalassiosiroid lineage, an age of at least 100 Ma seems most probable, in keeping with current molecular estimates that predict an origin for the clade between 125 and 149 Ma (Sörhannus, 2007).

Finally, we state with assurance that initial colonization of freshwater habitats by cyclostephanoid diatoms evolved from marine Thalassiosiraceae had occurred by 40 Ma, considerably earlier than longstanding biostratigraphic estimates placing these events in the Miocene (e.g., Krebs et al., 1987). Given the relative abundance of Cretaceous kimberlites in western and central North America (Heaman et al., 2004), as well as in southern Africa (Smith et al., 1985), concerted efforts should be directed at exploring their post-eruptive sedimentary fills for well-preserved early diatom floras. Given the results obtained thus far from Giraffe pipe sediments, the kimberlite maar depositional environment is likely to continue informing the fossil record of nonmarine diatoms.

FOOTNOTES

¹ The authors thank BHP Billiton Diamonds Inc. (Kelowna), the Geological Survey of Canada (Calgary), J. Westgate (University of Toronto), A. Lizarralde (Connecticut College), G. Braybrook (University of Alberta), and B. Perren (University of Toronto) for Greenland Puncticulata specimens. Comments by A. Alverson (Indiana University), M. Edlund (Science Museum of Minnesota), D. Harwood (University of Nebraska), two anonymous reviewers, and the editorial staff have greatly improved the manuscript. This work was supported by the Natural Sciences and Engineering Research Council (Canada) and the National Science Foundation (USA, NSF-DEB-0716606).

⁴ Author for correspondence (e-mail: awolfe{at}ualberta.ca)

LITERATURE CITED

Alverson, A. J. 2007. Strong purifying selection in the silicon transporters of marine and freshwater diatoms. Limnology and Oceanography 52: 1420–1429.[Web of Science]

Alverson, A. J., R. K. Jansen, AND E. C. Theriot. 2007. Bridging the Rubicon: Phylogenetic analysis reveals repeated colonizations of marine and fresh waters by thalassiosiroid diatoms. Molecular Phylogenetics and Evolution 45: 193–210.[CrossRef][Web of Science][Medline]

Armbrust, E. V., J. A. Berges, C. Bowler, B. R. Green, D. Martinez, N. H. Putnam, S. Zhou et al.. 2004. The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science 306: 79–86.[Abstract/Free Full Text]

Armbrust, E. V., AND H. M. Galindo. 2001. Rapid evolution of a sexual reproduction gene in centric diatoms of the genus Thalassiosira. Applied and Environmental Microbiology 67: 3501–3513.[Abstract/Free Full Text]

Chacón-Baca, E., H. Beraldi-Campesi, S. R. Cevallos-Ferriz, A. H. Knoll, AND S. Golubic. 2002. 70 Ma nonmarine diatoms from northern Mexico. Geology 30: 279–281.[Abstract/Free Full Text]

Creaser, R., H. Grütter, J. Carlson, AND B. Crawford. 2004. Macro crystal phlogopite Rb-Sr dates for the Ekati Property kimberlites, Slave Province, Canada: Evidence for multiple intrusive episodes in the Paleocene and Eocene. Lithos 76: 399–414.[CrossRef][Web of Science]

Edlund, M. B., C. M. Taylor, C. L. Schelske, AND E. F. Stoermer. 2000. Thalassiosira baltica (Grunow) Ostenfeld (Bacillariophyta), a new exotic species in the Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 57: 610–615.

Falkowski, P. G., M. Katz, A. H. Knoll, A. Quigg, J. A. Raven, O. Schofield, AND J. R. Taylor. 2004. The evolution of modern eukaryotic phytoplankton. Science 305: 354–360.[Abstract/Free Full Text]

Falkowski, P. G., AND J. A. Raven. 1997. Aquatic photosynthesis: Blackwell, Oxford, UK.

Fourtanier, E., F. Gasse, O. Bellier, M. G. Bonhomme, AND I. Robles. 1993. Miocene non-marine diatoms from the western Cordillera basins of northern Peru. Diatom Research 8: 13–30.

Fox, R., AND U. Sörhannus. 2003. RpoA: A useful gene for phylogenetic analysis in diatoms. Journal of Eukaryotic Microbiology 50: 471–475.[CrossRef][Web of Science][Medline]

Gersonde, R., AND D. M. Harwood. 1990. Lower Cretaceous diatoms from ODP leg 113 site 693 (Weddell Sea). Part 1: Vegetative cells. Proceedings of the Ocean Drilling Program, Scientific Results 113: 365–402.

Håkansson, H. 2002. A compilation and evaluation of species in the genera Stephanodiscus, Cyclostephanos and Cyclotella with a new genus in the family Stephanodiscaceae. Diatom Research 17: 1–139.[Web of Science]

Harrison, G. I., AND F. M. M. Morel. 1986. Response of the marine diatom Thalassiosira weissfiogii to iron stress. Limnology and Oceanography 31: 989–997.[Web of Science]

Harwood, D. M., V. A. Nikolaev, AND D. M. Winter. 2007. Cretaceous records of diatom evolution, radiation and expansion. In S. Starratt [ed.], Pond scum to carbon sink: Geological and environmental applications of the diatoms. Paleontological Society Papers vol. 13, 33–59.

Hasle, G. R., AND E. E. Syvertsen. 1985. Thalassiosiropsis, a new diatom genus from the fossil records. Micropaleontology 31: 82–91.[Abstract]

Heaman, L. M., B. A. Kjarsgaard, AND R. A. Creaser. 2004. The temporal evolution of North American kimberlites. Lithos 76: 377–397.[CrossRef][Web of Science]

Herth, W. 1978. A special chitin-fibril-synthesizing apparatus in the centric diatom Cyclotella. Die Naturwissenschaften 65: 260–261.[CrossRef][Web of Science]

Houk, V., AND R. Klee. 2004. The stelligeroid taxa of the genus Cyclotella (Kützing) de Brébisson (Bacillariophyceae) and their transfer into the new genus Discostella gen. nov. Diatom Research 19: 203–228.[Web of Science]

Kaczmarska, I., M. Beaton, A. C. Benoit, AND L. K. Medlin. 2006. Molecular phylogeny of selected members of the order Thalassiosirales (Bacillariopyta) and evolution of the fultoportula. Journal of Phycology 42: 121–138.[CrossRef][Web of Science]

Kaczmarska, I., AND J. M. Ehrman. 2008. Poloniasira fryxelliana Kaczmarska and Ehrman, a new thalassiosiroid diatom (Bacillariophyta) from the Lower Oligocene diatomites in Polish Flysch Carpatians, southeast Poland. Nova Hedwigia 133 (Beiheft):217–230.

Khursevich, G. 2006. Evolution of the extinct genera belonged to the family Stephanodiscaceae (Bacillariophyta) during the last eight million years in Lake Baikal. In N. Ognjanova-Rumenova, and K. Manoylov [eds.], Advances in phycological studies, Festschrift in honour of Prof. Dobrina Temniskova-Topalova, 73–89. Pensoft, Sofia, Bulgaria.

Kling, H. J., AND H. Håkansson. 1988. A light and electron microscope study of Cyclotella species (Bacillariophyceae) from central and northern Canada. Diatom Research 3: 55–82.

Kooistra, W. H. C. F., AND L. K. Medlin. 1996. Evolution of the diatoms (Bacillariophyta): IV. A reconstruction of their age from small subunit rRNA coding regions and the fossil record. Molecular Phylogenetics and Evolution 6: 391–407.[CrossRef][Web of Science][Medline]

Krammer, K., AND H. Lange-Bertalot. 1991. Bacillariophyceae 3. Teil: Centrales, Fragilariaceae, Eunotiaceae. In H. Ettl, J. Gerloff, H. Heynig, and D. Mollenhauer [eds.], Süßwasserflora von Mitteleuropa, vols. 2/3. G. Fischer Verlag, Jena, Germany.

Krebs, W. N., J. P. Bradbury, AND E. C. Theriot. 1987. Neogene and Quaternary lacustrine diatom biochronology, western U. S. A. Palaios 2: 505–513.[Abstract/Free Full Text]

Roberts, K., E. Granum, R. C. Leegood, AND J. A. Raven. 2007. C₃ and C₄ pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiology 145: 230–235.[Abstract/Free Full Text]

Round, F. E., R. M. Crawford, AND D. G. Mann. 1990. The diatoms—Biology and morphology of the genera. Cambridge University Press, Cambridge, UK.

Rouse, G. E. 1977. Paleogene palynomorph ranges in western and northern Canada. In W. D. Elsik [ed.], Contributions of stratigraphic palynology: Cenozoic palynology 1, 48–65. American Association of Stratigraphic Palynologists, Dallas, Texas, USA.

Rueter, J. G., AND F. M. M. Morel. 1981. The interaction between zinc deficiency and copper toxicity as it affects the silicic acid uptake mechanisms in Thalassiosira pseudonana. Limnology and Oceanography 26: 67–73.[Web of Science]

Schneider, H., E. Schuettpelz, K. M. Pryer, R. Cranfill, S. Magallón, AND R. Lupia. 2004. Ferns diversified in the shadow of angiosperms. Nature 428: 553–557.[CrossRef][Medline]

Sims, P. A., D. G. Mann, AND L. K. Medlin. 2006. Evolution of the diatoms: Insights from fossil, biological and molecular data. Phycologia 45: 361–402.[CrossRef][Web of Science]

Sinninghe Damsté, J. S., G. Muyzer, B. Abbas, S. W. Rampen, G. Masse, W. G. Allard, S. T. Belt et al.. 2004. The rise of the rhizosolenid diatoms. Science 304: 584–587.[Abstract/Free Full Text]

Siver, P. A., P. B. Hamilton, K. Stachura-Suchoples, AND J. P. Kociolek. 2005. Diatoms of North America: The freshwater flora of Cape Cod, Massachusetts, USA. H. Lange-Bertalot [ed.], Iconographia diatomologica, vol. 14. Koeltz Scientific Books, Koeningstein, Liechtenstein.

Siver, P. A., AND A. P. Wolfe. 2005. Eocene scaled chrysophytes with pronounced modern affinities. International Journal of Plant Sciences 166: 533–536.[CrossRef][Web of Science]

Siver, P. A., AND A. P. Wolfe. 2007. Eunotia spp. (Bacillariophyceae) from Middle Eocene lake sediments and comments on the origin of the diatom raphe. Canadian Journal of Botany 85: 83–90.[CrossRef]

Skvortzow, B. V. 1937. Diatoms from Lake Michigan I. American Midland Naturalist 18: 652–658.[CrossRef]

Smith, C. B., H. L. Allsopp, J. D. Kramers, G. Hutchinson, AND J. C. Roddick. 1985. Emplacement ages of Jurassic-Cretaceous South African kimberlites by the Rb-Sr method on phlogopite and whole-rock samples. South African Journal of Geology 88: 249–266.[Abstract]

Sörhannus, U. 2004. Diatom phylogenetics inferred based on direct optimization of nuclear-encoded SSU rRNA sequences. Cladistics 20: 487–497.[CrossRef][Web of Science]

Sörhannus, U. 2007. A nuclear-encoded small-subunit ribosomal RNA timescale for diatom evolution. Marine Micropaleontology 65(1–2): 1–12. doi:.[CrossRef][Web of Science]

Theriot, E. C. 2008. Applications of phylogenetic principles to testing evolutionary scenarios: A comment on Kaczmarska et al. "Molecular phylogeny of selected members of the order Thalassiosirales (Bacillariophyta) and evolution of the fultoportula. Journal of Phycology 44: 821–833.[CrossRef][Web of Science]

Theriot, E. C., S. C. Fritz, C. Whitlock, AND D. J. Conley. 2006. Late-Quaternary rapid morphological evolution of an endemic diatom in Yellowstone Lake, Wyoming. Paleobiology 32: 38–54.[Abstract/Free Full Text]

Walsby, A. E., AND A. Xypolyta. 1977. The form resistance of chitan fibres attached to the cells of Thalassiosira fluviatilis Hustedt. British Phycological Journal 12: 215–223.[CrossRef][Web of Science]

Wolfe, A. P., M. B. Edlund, A. R. Sweet, AND S. Creighton. 2006. A first account of organelle preservation in Eocene nonmarine diatoms: Observations and paleobiological implications. Palaios 21: 298–304.[Abstract/Free Full Text]

CiteULike    Complore    Connotea    Del.icio.us    Digg    Facebook    Reddit    Technorati    Twitter    What's this?

This Article Abstract Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Wolfe, A. P. Articles by Siver, P. A. Search for Related Content PubMed Articles by Wolfe, A. P. Articles by Siver, P. A. Agricola Articles by Wolfe, A. P. Articles by Siver, P. A. Social Bookmarking                            What's this?