Plant Ecology and Evolution 152(2): 262-284, doi: 10.5091/plecevo.2019.1604
Morphological reconsideration of the araphid genus Pseudostaurosira (Bacillariophyceae), a revision of Gedaniella, Popovskayella and Serratifera, and a description of a new Nanofrustulum species
expand article infoEduardo Antonio Morales Luizaga, Carlos E. Wetzel§, Maria Helena Novais|, Krisztina Buczkó, M. Manuela Morais|, Luc Ector#
‡ University of Évora, Évora, Portugal§ Environmental Research and Innovation Department (ERIN) Institute of Science and Technology (LIST), 41 rue du Brill, 4422 Belvaux, Luxembourg| Water Laboratory, University of Évora, Rua da Barba Rala No. 1, Parque Industrial e Tecnológico, Évora 7005-345, Portugal¶ Department of Botany, Hungarian Natural History Museum, Könyves Kálmán krt. 40, 1087, Budapest and MTA Centre for Ecological Research, Danube Research Institute, Karolina St 29, 1113 Budapest, Hungary# Luxembourg Institute of Science and Technology, Belvaux, Luxembourg
Open Access

Background and aims – As a result of the description of many new species, reanalyses of type material, and information becoming available on valve morphogenesis in small araphid diatoms lacking a rimoportulae, the existing classification scheme at the genus level needs revision. Because morphological information has increased manyfold since the system provided by Williams & Round (1987), it may now be possible to find distinguishing characters in order to produce a more stable and useful framework, encompassing a morphogenetic perspective, which could then guide the placement of newly discovered taxa. This new framework could also be used to help assess the molecular information generated for the group, based on which many new genera are being erected, but perhaps without proper pondering of morphological data.

Methods – A thorough review was made of available published information on the ultrastructure of small-celled araphid diatoms lacking rimoportulae. In addition, image databases were searched, and new light and scanning electron microscopical observations made of some hitherto undescribed species.

Key results and conclusions – We provide a table of putative distinguishing features for nine genera (Nanofrustulum, Opephora, Pseudostaurosira, Pseudostaurosiropsis, Punctastriata, Sarcophagodes, Stauroforma, Staurosira and Staurosirella), together with a discussion on their value for discriminating these small diatoms using a morphogenetic perspective. Based on our findings, we amend the genus Pseudostaurosira, establishing wide and short vimines as its most characteristic feature. We use our system in describing a new species from Bolivia, which we place in Nanofrustulum based on its quasifract copulae, the distinguishing trait of the genus. The new species is distinguished from its congeners by its heteropolar valves, apical pore field features, and the multiseriate areolae. We also examine the three genera Popovskayella, Gedaniella, and Serratifera, the latter two recently erected based on molecular information. Since none of these latter genera pass the morphogenetic evaluation we think is essential, we place them in synonymy with other genera and provide the consequent nomenclatural changes. Finally, we make several new combinations in Nanofrustulum, Pseudostaurosira, Sarcophagodes and Staurosirella.

Araphids, Bolivian Altiplano, Fragilariaceae, molecular phylogenies, Pantocsek, systematics, type material


  • Aitken Z.H., Luo S., Reynolds S.N., Thaulow C., Greer J.R. (2016) Microstructure provides insights into evolutionary design and resilience of Coscinodiscus sp. frustule. Proceedings of the National Academy of Sciences of the United States of America 113: 2017–2022.
  • Barber H.G., Haworth E.Y. (1981) A guide to the morphology of the diatom frustule. With a key to the British Freshwater genera. Freshwater Biological Association, Ambleside. Scientific Publication No. 44: 1–112.
  • Cejudo-Figueiras C., Morales E.A., Wetzel C.E., Blanco S., Hoffmann L., Ector L. (2011) Analysis of the type of Fragilaria construens var. subsalina (Bacillariophyceae) and description of two morphologically related taxa from Europe and the United States. Phycologia 50: 67–77.
  • Cleve P.T., Möller J.D. (1879) Diatoms. Part V, No. 217–276. Upsala, Esatas Edquists Boktryckeri.
  • Compère P. (2001) Ulnaria (Kützing) Compère, a new genus name for Fragilaria subgen. Alterasynedra Lange-Bertalot with comments on the typification of Synedra Ehrenberg. In: Jahn R., Kociolek J.P., Witkowski A., Compère P. (eds) Lange-Bertalot-Festschrift. Studies on diatoms dedicated to Prof. Dr. Dr. h.c. Horst Lange-Bertalot on the occasion of his 65th birthday: 97–101. Ruggell, A.R.G. Gantner Verlag K.G.
  • Cox E.J. (2004) Pore occlusions in raphid diatoms - a reassessment of their structure and terminology, with particular reference to members of the Cymbellales. Diatom 20: 33–46.
  • Cox E.J. (2010) Morphogenetic information and the selection of taxonomic characters for raphid diatom systematics. Plant Ecology and Evolution 143: 271–277.
  • Cox E.J. (2012) Ontogeny, homology, and terminology-wall morphogenesis as an aid to character recognition and character state definition for pennate diatom systematics. Journal of Phycology 48: 1–31.
  • Cox E.J., Kennaway G.M. (2004) Studies of valve morphogenesis in pennate diatoms: investigating aspects of cell biology in a systematic context. In: Poulin M. (ed.) Proceedings of the Seventeenth International Diatom Symposium. Ottawa, Canada, 25th–31st August 2002: 35–48. Bristol, Biopress Limited.
  • Cox E.J., Ross R. (1981) The striae of pennate diatoms. In: Ross R. (ed.) Proceedings of the Sixth Symposium on Recent and Fossil Diatoms, Budapest, September 1–5, 1980: 267–278. Koenigstein, Otto Koeltz - Science Publishers.
  • Edlund M.B., Morales E.A., Spaulding S.A. (2006) The type and taxonomy of Fragilaria elliptica Schumann, a widely misconstrued taxon. In: Witkowski A. (ed.) Proceedings of the Eighteenth International Diatom Symposium. Międzydroje, Poland, 2nd–7th September 2004: 53–59. Bristol, Biopress Limited.
  • Flower R.J., Jones V.J., Round F.E. (1996) The distribution and classification of the problematic Fragilaria (virescens v.) exigua Grun. / Fragilaria exiguiformis (Grun.) Lange-Bertalot: a new species or a new genus? Diatom Research 11: 41–57.
  • Frankovich T.A., Sullivan M.J., Stacy N.I. (2015) Three new species of Tursiocola (Bacillariophyta) from the skin of the West Indian manatee (Trichechus manatus). Phytotaxa 204: 33–48. https://
  • Frankovich T.A., Ashworth M.P., Sullivan M.J., Theriot E.C., Stacy N.I. (2018) Epizoic and apochlorotic Tursiocola species (Bacillariophyta) from the skin of Florida manatees (Trichechus manatus latirostris). Protist 169: 539–568.
  • Frenguelli J. (1945) XIX contribución al conocimiento de las diatomeas argentinas. Las diatomeas del Platense. Revista del Museo de La Plata, Nueva Serie, Sección Paleontología 3(16): 77–221, pls 1–15.
  • García M.L., Maidana N.I., Ector L., Morales E.A. (2017) Staurosira patagonica sp. nov., a new diatom (Bacillariophyta) from southern Argentina, with a discussion on the genus Staurosira Ehrenberg. Nova Hedwigia, Beiheft 146: 103–123.
  • Genkal S.I., Bondarenko N.A., Shchur L.A. (2011) Diatoms of lakes in south and north of the Eastern Siberia. Rybinsk, Rybinsky Dom Pechati. (In Russian).
  • Goldenberg Vilar A., van Dam H., van Loon E.E., Vonk J.A., van der Geest H., Admiraal W. (2014) Eutrophication decreases distance decay of similarity in diatom communities. Freshwater Biology 59: 1522–1531. https://
  • Grana L., Morales E.A., Maidana N.I., Ector L. (2018) Two new species of Staurosira and Pseudostaurosira (Bacillariophyta) from the highlands of Argentina (south-central Andes) and two new nomenclatural combinations. Phytotaxa 365: 60–72.
  • Guiry M.D., Guiry G.M. (2018) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from [accessed 25 Jul. 2018].
  • Hamilton P.B., Siver P.A. (2008) The type for Fragilaria lancettula Schumann 1867 and transfer to the genus Punctastriata as P. lancettula (Schum.) Hamilton & Siver comb. nov. Diatom Research 23: 355–365.
  • Hegewald E., Silva P.C. (1988) Annotated catalogue of Scenedesmus and nomenclaturally related genera, including original descriptions and figures. Bibliotheca Phycologica 80: 1–587.
  • Hustedt F. (1938) Systematische und ökologische Untersuchungen über die Diatomeen-Flora von Java, Bali und Sumatra nach dem Material der Deutschen Limnologischen Sunda-Expedition. Systematischer Teil I. Archiv für Hydrobiologie, Supplement-Band 15: 131–177.
  • Kociolek J.P., Williams D.M. (2015) How to define a diatom genus? Notes on the creation and recognition of taxa, and a call for revisionary studies of diatoms. Acta Botanica Croatica 74: 195–210.
  • Kociolek J.P., Laslandes B., Benett D., Thomas E., Brady M., Graeff C. (2014) Diatoms of the United States 1. Taxonomy, ultrastructure and descriptions of new species and other rarely reported taxa from lake sediments in the western U.S.A. Bibliotheca Diatomologica 61: 1–188.
  • Krammer K., Lange-Bertalot H. (1991) Bacillariophyceae 3. Teil: Centrales, Fragilariaceae, Eunotiaceae. In: Ettl H., Gerloff J., Heynig H., Mollenhauer D. (eds) Süßwasserflora von Mitteleuropa 2/4: 1–576. Stuttgart, Gustav Fischer Verlag.
  • Kulikovskiy M.S., Lange-Bertalot H., Kuznetsova I.V. (2015) Lake Baikal: Hotspot of endemic diatoms II. Iconographia Diatomologica 26: 1–656.
  • Lange-Bertalot H. (1989) Können Staurosirella, Punctastriata und weitere Taxa sensu Williams & Round als Gattungen der Fragilariaceae kritischer Prüfung standhalten? Generic rank for Punctastriata, Staurosirella and other taxa sensu Williams & Round? Nova Hedwigia 49: 79–106.
  • Lange-Bertalot H. (1993) Once more: Staurosirella, Punctastriata etc. A reply to Round & Williams (1992). Nova Hedwigia 56: 179–182.
  • Lange-Bertalot H., Genkal S.I. (1999) Diatomeen aus Sibirien I. Inseln im Arktischen Ozean (Yugorsky-Shar Strait) [Diatoms from Siberia I. Islands in the Arctic Ocean (Yugorsky-Shar Strait)]. Iconographia Diatomologica 6: 1–271.
  • Lange-Bertalot H., Hofmann G., Werum M., Cantonati M. (2017) Freshwater benthic diatoms of Central Europe: Over 800 common species used in ecological assessment. English edition with updated taxonomy and added species. Edited by Cantonati M., Kelly M.G., Lange-Bertalot H. Schmitten-Oberreifenberg, Koeltz Botanical Books.
  • Lee J.J., Reimer Ch.W., McEnery, M.E. (1980) The identification of diatoms isolated as endosymbionts from larger foraminifera from the Gulf of Eilat (Red Sea) and the description of 2 new species, Fragilaria shiloi sp. nov. and Navicula reissii sp. nov. Botanica Marina 23: 41–48.
  • Li C.L., Ashworth M.P., Witkowski A., Lobban C.S., Zgłobicka I., Kurzydłowski K.J., Qin S. (2016) Ultrastructural and molecular characterization of diversity among small araphid diatoms all lacking rimoportulae. I. Five new genera, eight new species. Journal of Phycology 52: 1018–1036.
  • Li C.L., Witkowski A., Ashworth M.P., Dąbek P., Sato S., Zgłobicka I., Witak M., Khim J.S., Kwon C.-J. (2018) The morphology and molecular phylogenetics of some marine diatom taxa within the Fragilariaceae, including twenty undescribed species and their relationship to Nanofrustulum, Opephora and Pseudostaurosira. Phytotaxa 355: 1–104.
  • Lilitskaya G.G. (2016) Bacillariophyta of small water bodies of Kiev (Ukraine). 2. Araphid diatoms: Fragilariaceae, Diatomaceae, and Tabellariaceae. International Journal on Algae 18: 225–246.
  • Mann D.G. (1984) An ontogenetic approach to diatom systematics. In: Mann D.G. (ed.) Proceedings of the Seventh International Diatom Symposium Philadelphia, August 22–27, 1982: 113–144. Koenigstein, Otto Koeltz.
  • Mann D.G. (2006) Specifying a morphogenetic model for diatoms: an analysis of pattern faults in the Voigt zone. Nova Hedwigia, Beiheft 130: 97–118.
  • Mann D.G. (2010) Discovering diatom species: is a long history of disagreements about species-level taxonomy now at an end? Plant Ecology and Evolution 143: 251–264.
  • Marciniak B. (1982) Late Glacial and Holocene new diatoms from a glacial Lake Przedni Staw in the Pięć Stawów Polskich Valley, Polish Tatra Mts. Acta Geologica Academiae Scientiarum Hungaricae 25: 161–171.
  • Marciniak B. (1986) Late Glacial Fragilaria flora from lake sediments of the Tatra Mts. and the Alps. In: Round F.E. (ed.) Proceedings of the Ninth International Diatom Symposium. Bristol, August 24–30, 1986: 233–243. Bristol, Biopress Ltd. and Koenigstein, Koeltz Scientific Books.
  • Medlin L., Desdevises, Y. (2016) Phylogeny of ‘araphid’ diatoms inferred from SSU and LSU rDNA, RBCL and PSBA sequences. Vie et Milieu 66: 129–154.
  • Medlin L., Williams D.M., Sims P.A. (1993) The evolution of the diatoms (Bacillariophyta). I. Origin of the group and assessment of the monophyly of its major divisions. European Journal of Phycology 28: 261–275.
  • Medlin L., Jung I., Bahulikar R., Mendgen K., Kroth P., Kooistra W.H.C.F. (2008) Evolution of the diatoms. VI. Assessment of the new genera in the araphids using molecular data. Nova Hedwigia, Beiheft 133: 81–100.
  • Medlin L., Yang I., Sato S. (2012) Evolution of the diatoms. VII. Four gene phylogeny assesses the validity of selected araphid genera. Nova Hedwigia, Beiheft 141: 505–514.
  • Metzeltin D., Lange-Bertalot H. (1998) Tropische Diatomeen in Südamerika I. 700 überwiegend wenig bekannte oder neue Taxa repräsentativ als Elemente der neotropischen Flora [Tropical diatoms of South America I. About 700 predominantly rarely known or new taxa representative of the neotropical flora]. Iconographia Diatomologica 5: 1–695.
  • Morales E.A. (2001) Morphological studies in selected fragilarioid diatoms (Bacillariophyceae) from Connecticut waters (U.S.A.). Proceedings of the Academy of Natural Sciences of Philadelphia 151: 105–120.
  • Morales E.A. (2002) Studies in selected fragilarioid diatoms of potential indicator value from Florida (USA) with notes on the genus Opephora Petit (Bacillariophyceae). Limnologica 32: 102–113.
  • Morales E.A. (2003) On the taxonomic status of the genera Belonastrum and Synedrella proposed by Round and Maidana (2001). Cryptogamie Algologie 24: 277–288.
  • Morales E.A. (2006) Staurosira incerta (Bacillariophyceae) a new fragilarioid taxon from freshwater systems in the United States with comments on the structure of girdle bands in Staurosira Ehrenberg and Staurosirella Williams et Round. In: Ognjanova-Rumenova N., Manoylov K. (eds) Advances in Phycological Studies. Festschrift in Honour of Prof. Dobrina Temniskova-Topalova: 133–145. Sofia-Moscow, Pensoft Publishers & University Publishing House.
  • Morales E.A., Edlund M.B. (2003) Studies in selected fragilarioid diatoms (Bacillariophyceae) from Lake Hovsgol, Mongolia. Phycological Research 51: 225–239.
  • Morales E.A., Manoylov K.M. (2006a) Morphological studies on selected taxa in the genus Staurosirella Williams et Round (Bacillariophyceae) from rivers in North America. Diatom Research 21: 343–364.
  • Morales E.A., Manoylov K.M. (2006b) Staurosirella incognita Morales et Manoylov sp. nov., a non-spiny species from North America, with an emended description of Staurosirella Williams et Round (Bacillariophyceae). In: Witkowski A. (ed.) Proceedings of the Eighteenth International Diatom Symposium. Międzyzdroje, Poland, 2nd–7th September 2004: 325–336. Bristol, Biopress Limited.
  • Morales E.A., Edlund M.B., Spaulding S.A. (2010a) Description and ultrastructure of araphid diatom species (Bacillariophyceae) morphologically similar to Pseudostaurosira elliptica (Schumann) Edlund et al. Phycological Research 58: 97–107.
  • Morales E.A., Manoylov K.M., Bahls L.L. (2010b) Three new araphid diatoms (Bacillariophyta) from rivers in North America. Proceedings of the Academy of Natural Sciences of Philadelphia 160: 29–46.
  • Morales E.A., Wetzel C.E., Ector L. (2010c) Two short-striated species of Staurosirella (Bacillariophyceae) from Indonesia and the United States. Polish Botanical Journal 55: 107–117.
  • Morales E.A., Novais M.H., Chávez G., Hoffmann L., Ector L. (2012) Diatoms (Bacillariophyceae) from the Bolivian Altiplano: three new araphid species from the Desaguadero River draining Lake Titicaca. Fottea 12: 41–58.
  • Morales E.A., Guerrero J.M., Wetzel C.E., Sala S., Ector L. (2013) Unraveling the identity of Fragilaria pinnata Ehrenberg and Staurosira pinnata Ehrenberg: research in progress on a convoluted story. Cryptogamie Algologie 34: 89–102.
  • Morales E.A., Buczkó K., Wetzel C.E., Novais M.H., Ognjanova-Rumenova N., Hoffmann L., Ector L. (2014a) Transfer of Staurosira grunowii to Staurosirella. Diatom Research 29: 105–110.
  • Morales E.A., Rivera S.F., Wetzel C.E., Novais M.H., Hamilton P.B., Hoffmann L., Ector L. (2014b) New epiphytic araphid diatoms in the genus Ulnaria (Bacillariophyta) from Lake Titicaca, Bolivia. Diatom Research 29: 41–54.
  • Morales E.A., Wetzel C.E., Rivera S.F., Van de Vijver B., Ector L. (2014c) Current taxonomic studies on the diatom flora (Bacillariophyceae) of the Bolivian Altiplano, South America, with possible consequences for palaeoecological assessments. Journal of Micropalaeontology 33: 121–129.
  • Morales E.A., Wetzel C.E., Van de Vijver B., Ector L. (2015) Morphological studies on type material of widely cited araphid diatoms (Bacillariophyta). Phycologia 54: 455–470.
  • Moser G. (1999) Die Diatomeenflora von Neukaledonien. Bibliotheca Diatomologica 43: 1–205.
  • Ognjanova-Rumenova N., Temniskova-Topalova D., Valeva M. (1994) Ultrastructure of Fragilaria Lyngbye species (Bacillariophyta) from Neogene sediments in Bulgaria. In: Kociolek J.P. (ed.) Proceedings of the 11th International Diatom Symposium. San Francisco, California 12–17 August 1990: 291–300. San Francisco, California Academy of Science.
  • Pantocsek J. (1913) A lutillai ragpalában elöforduló Bacillariák vagy Kovamoszatok leírása [Bacillarien des Klebschiefers von Lutilla]. A pozsonyi Orvos-Természettudományi Egyesület közleményei [Verhandlungen des Vereins für Natur-und Heilkunde zu Pozsony, Neue Folge] 23: 19–35, 2 pls. Pozsonyban, Wigand K.F. könyvnyomdája.
  • Pickett-Heaps J.D. (1998) Cell division and morphogenesis of the centric diatom Chaetoceros decipiens (Bacillariophyceae) II. Electron microscopy and a new paradigm for tip growth. Journal of Phycology 34: 995–1004.
  • Round F.E., Crawford R.M., Mann D.G. (1990) Diatoms: biology and morphology of the genera. Cambridge, Cambridge University Press.
  • Rumrich U., Lange-Bertalot H., Rumrich M. (2000) Diatomeen der Anden. Von Venezuela bis Patagonien/Feuerland [Diatom from the Andes. From Venezuela to Patagonia/Tierra del Fuego]. Iconographia Diatomologica 9: 1–649.
  • Sabbe K., Vyverman W. (1995) Taxonomy, morphology and ecology of some widespread representatives of the diatom genus Opephora. European Journal of Phycology 30: 235–249.
  • Sato S., Mann D.G., Matsumoto S., Medlin L.K. (2008) Pseudostriatella (Bacillariophyta): a description of a new araphid diatom genus based on observations of frustule and auxospore structure and 18S rDNA phylogeny. Phycologia 47: 371–391.
  • Sato S., Matsumoto S., Medlin L.K. (2009) Fine structure and 18S rDNA phylogeny of a marine araphid pennate diatom Plagiostriata goreensis gen. et sp. nov. (Bacillariophyta). Phycological Research 57: 25–35.
  • Takano H. (1986) A new diatom in the genus Fragilaria from shallow waters in Mikawa Bay, Japan. Bulletin of the Tokai Regional Fisheries Research Laboratory 120: 27–37.
  • Takano H. (1988) Two new diatoms found in marine waters of Japan. Bulletin of the Tokai Regional Fisheries Research Laboratory 125: 33–44.
  • Talgatti D., Wetzel C.E., Morales E.A., Ector L., Torgan L.C. (2014) Transfer of Fragilaria atomus Hust. to the genus Stauroforma (Bacillariophyta) based on observation of type and newly collected material. Phytotaxa 158: 43–56.
  • Theriot E.C. (2008) Application 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.
  • Theriot E.C., Ashworth M., Ruck E., Nakov T., Jansen R.K. (2010) A preliminary multigene phylogeny of the diatoms (Bacillario­phyta): challenges for future research. Plant Ecology and Evolution 143: 278–296.
  • Tiffany M.A. (2015) Valve and girdle band morphogenesis in the pseudocellate diatom species Biddulphia biddulphiana J.E. Smith (Boyer) and Isthmia nervosa Kütz. Nova Hedwigia, Beiheft 144: 61–95.
  • Van de Vijver B., Frenot Y., Beyens L. (2002) Freshwater diatoms from Ile de la Possession (Crozet Archipelago, Subantarctica). Bibliotheca Diatomologica 46: 1–412.
  • Wetzel C.E., Morales E.A., Blanco S., Ector L. (2013) Pseudostaurosira cataractarum comb. nov. (Bacillariophyta): type analysis, ecology and world distribution of a former “centric” diatom. Acta Nova 6: 53–63.
  • Witkowski A. (1993) Fragilaria gedanensis sp. nov. (Bacillariophyceae), a new epipsammic diatom species from the Baltic Sea. Nova Hedwigia 56: 497–503.
  • Witkowski A. (1994) Recent and fossil diatom flora of the Gulf of Gdańsk, Southern Baltic Sea. Origin, composition and changes of diatom assemblages during the Holocene. Bibliotheca Diatomologica 28: 1–313.
  • Witkowski A., Lange-Bertalot H. (1993) Established and new diatom taxa related to Fragilaria schulzii Brockmann. Limnologica 23: 59–70.
  • Witkowski A., Lange-Bertalot H., Witak M. (1995) Diatom taxa of unusual frustule structure belonging to the genus Fragilaria. Fragmenta Floristica et Geobotanica 40: 729–741.
  • Witkowski A., Lange-Bertalot H., Metzeltin D. (2000) Diatom flora of marine coasts I. Iconographia Diatomologica 7: 1–925.
  • Witkowski A., Riaux-Gobin C., Daniszewska-Kowalczyk G. (2010) New marine littoral diatom species (Bacillariophyta) from Kerguelen Islands. II. Heteropolar species of Fragilariaceae. Vie et Milieu 60: 265–281.