A new approach for identification of the genus Paralia (Bacillariophyta) in Korea based on morphology and morphometric analyses

  • cc icon
  • ABSTRACT

    Paralia species have been frequently reported as P. sulcata in Korea, despite the species diversity within the genus. To understand the species diversity of Paralia in Korea, we collected phytoplankton samples at 79 sites from April 2006 to April 2015. Five Paralia species, P. fenestrata, P. guyana, P. marina, P. cf. obscura, and P. sulcata, were observed during this study, and we described their fine structure in terms of quantitative and qualitative morphological characteristics. To provide additional criteria to identify Paralia species more clearly, we morphometrically analysed four quantitative characteristics on valve diameter: pervalvar axis / diameter, internal linking spines / diameter, marginal linking spines / diameter, and fenestrae/diameter using non-metric multidimensional scaling (MDS). MDS analysis distinguished four Paralia species: P. guyana, P. marina, P. cf. obscura, and P. sulcata, with the exception of P. fenestrata. This new approach in using morphometric analysis is useful for the accurate identification of Paralia species.


  • KEYWORD

    diatom , morphometric analysis , non-metric multidimensional scaling (MDS) , Paralia , taxonomy

  • 1. Clarke K. R. 1993 Non-parametric multivariate analyses ofchanges in community structure [Aust. J. Ecol.] Vol.18 P.117-143 google doi
  • 2. Clarke K. R., Ainsworth M. 1993 A method of linking multivariate community structure to environmental variables [Mar. Ecol. Prog. Ser.] Vol.92 P.205-219 google doi
  • 3. Clarke K. R., Warwick R. M. 2001 Changes in marine communities: an approach to statistical analysis and interpretation P.172 google
  • 4. Cleve P. T. 1873 On diatoms from the Arctic Sea P.1-28 google
  • 5. Crawford R. M. 1979 Taxonomy and frustular structure of the marine centric diatom Paralia sulcata [J. Phycol.] Vol.15 P.200-210 google doi
  • 6. Crawford R. M., Sims P. A., Hajos M. 1990 The morphology and taxonomy of the centric diatom genus Paralia. I. Paralia siberica comb. nov. [Diatom Res.] Vol.5 P.241-252 google doi
  • 7. Droop S. J. M. 1994 Morphological variation in Diploneis smithii and D. fusca (Bacillariophyceae) [Arch. Protistenkd] Vol.144 P.249-270 google doi
  • 8. Droop S. J. M., Mann D. G., Lokhorst G. M. 2000 Spatial and temporal stability of demes in Diploneis smithii D.fusca (Bacillariophyta) supports a narrow species concept [Phycologia] Vol.39 P.527-546 google doi
  • 9. Ehrenberg C. G. 1838 Die Infusionshierchen als vollkommene Organismen: Ein Blick in das tiefere organische Leben der Natur P.548 google
  • 10. Field J. G., Clarke K. R., Warwick R. M. 1982 A practical strategy for analysing multispecies distribution patterns [Mar. Ecol. Prog. Ser.] Vol.8 P.37-52 google doi
  • 11. Garcia M., Talgatti D., Souza-Mosimann R., Laudares-Silva R. 2012 Morphology and distribution of Paralia Heiberg (Coscinodiscophyceae) in southern Brazil [Iheringia Ser. Bot.] Vol.67 P.225-235 google
  • 12. Goldman N., Paddock T. B. B., Shak K. M. 1990 Quantitative analysis of shape variation in populations of Surirella fastuosa [Diatom Res.] Vol.5 P.25-42 google doi
  • 13. Grunow A. 1884 Die Diatomeen von Franz Josefs-Land [enkschriften der Kaiserlichen Akademie der Wissenschaften] Vol.48 P.53-112 google
  • 14. Guiry M. D., Guiry G. M. 2016 AlgaeBase google
  • 15. Hajos S. M. 1973 Faciological and stratigraphic importance of the Miocene diatoms in Hungary [Nova Hedwig. Beih.] Vol.45 P.365-376 google
  • 16. Hasle G. R., Fryxell G. A. 1970 Diatoms: cleaning and mounting for light and electron microscopy [Trans. Am. Microsc. Soc.] Vol.89 P.469-474 google doi
  • 17. Heiberg P. A. C. 1863 Conspectus criticus diatomacearum danicarum P.135 google
  • 18. Janisch C. 1862 Zur charakteristik des Guano’s von verschieden Fundorten P.1-29 google
  • 19. Konno S., Jordan R. W., Likhoshway Y. 2008 Paralia longispina sp. nov., an extant species from Palau and Haha-jima, western North Pacific [Proc. 19th Int. Diatom Symp.] P.55-69 google
  • 20. Kutzing F. T. 1844 Die Kieselschaligen. Bacillarien oder Diatomeen P.152 google
  • 21. Loseva E. I., Simola H. 1988 The valve ultrastructure of fossil Paralia sulcata (Bacillariophyceae) [Proc. 10th Int. Diatom Symp.] P.83-91 google
  • 22. MacGillivary M. L., Kaczmarska I. 2012 Genetic differentiation within the Paralia longispina (Bacillariophyta) species complex [Botany] Vol.90 P.205-222 google doi
  • 23. MacGillivary M. L., Kaczmarska I. 2013 Lectotypification of Paralia sulcata and description of P. obscura sp. nov. (Bacillariophyta) from the Ehrenberg Collection [Diatom Res.] Vol.28 P.221-235 google doi
  • 24. MacGillivary M. L., Kaczmarska I. 2015 Paralia (Bacillariophyta) stowaways in ship ballast: implications for biogeography and diversity of the genus [J. Biol. Res. Thessalon.] Vol.22 P.2 google doi
  • 25. McQuoid M. R., Nordberg K. 2003 The diatom Paralia sulcata as an environmental indicator species in coastal sediments [Estuar. Coast. Shelf. Sci.] Vol.56 P.339-354 google doi
  • 26. Mou D., Stoermer E. F. 1992 Separating Tabellaria (Bacillariophyceae) shape groups based on Fourier descriptors [J. Phycol.] Vol.28 P.386-395 google
  • 27. Pappas J. L., Fowler G. W., Stoermer E. F. 2001 Calculating shape descriptors from Fourier analysis: shape analysis of Asterionella (Heterokontophyta, Bacillariophyceae) [Phycologia] Vol.40 P.440-456 google doi
  • 28. Pappas J. L., Stoermer E. F. 2003 Legendre shape descriptors and shape group determination of specimens in the Cymbella cistula species complex [Phycologia] Vol.42 P.90-97 google doi
  • 29. ?ehakova Z. 1975 Marine diatoms in Helvetian sediments of the central Paratethys [Nova Hedwig. Beih.] Vol.53 P.293-308 google
  • 30. Rhode K. M., Pappas J. L., Stormer E. F. 2001 Quantitative analysis of shape variation in type and modern populations of Meridion (Bacillariophyceae) [J. Phycol.] Vol.37 P.175-183 google doi
  • 31. Round F. E., Crawford R. M., Mann D. G. 1990 The diatoms: biology and morphology of the genera P.747 google
  • 32. Sawai Y., Nagumo T., Toyoda K. 2005 Three extant species of Paralia (Bacillariophyceae) along the coast of Japan [Phycologia] Vol.44 P.517-529 google doi
  • 33. Schmidt A. 1959 Atlas der Diatomaceen-Kunde P.1976 google
  • 34. Schneider C. A., Rasband W. S., Eliceiri K. W. 2012 NIH Image to ImageJ: 25 years of image analysis [Nat. Methods] Vol.9 P.671-675 google doi
  • 35. Simonsen R. 1974 The diatom plankton of the Indian Ocean Expedition of R/V “Meteor” 1964-1965. “Meteor” Forsch [Ergeb.] Vol.19 P.1-107 google
  • 36. Sims P. A., Crawford R. M. 2002 The morphology and taxonomy of the marine centric diatom genus Paralia. II. Paralia crenulata, P. fausta and the new species, P. hendeyi [Diatom Res.] Vol.17 P.363-382 google doi
  • 37. Smith W. 1856 A synopsixs of the British Diatomaceae. II P.104 google
  • 38. Stabell B. 1996 Paralia thybergii sp. nov.: another fossil Paralia [Diatom Res.] Vol.11 P.155-163 google doi
  • 39. Steinman A. D., Ladewski T. B. 1987 Quantitative shape analysis of Eunotia pectinalis (Bacillariophyceae) and its application to seasonal distribution patterns [Phycologia] Vol.26 P.467-477 google doi
  • 40. Stoermer E. F., Ladewski T. B. 1982 Quantitative analysis of shape variation in type and modern populations of Gomphoneis herculeana [Nova Hedwig. Beih.] Vol.73 P.347-386 google
  • 41. Stoermer E. F., Qi Y. -Z., Ladewski T. B. 1986 A quantitative investigation of shape variation in Didymosphenia (Lyngbye) M. Schmidt (Bacillariophyta) [Phycologia] Vol.25 P.494-502 google doi
  • 42. Theriot E., Ladewski T. B. 1986 Morphometric analysis of shape of specimens from the neotype of Tabellaria flocculosa (Bacillariophyceae) [Am. J. Bot.] Vol.73 P.224-229 google doi
  • [Table 1.] Comparison of some morphological features and biometric data of Paralia species from Korean coastal waters
    Comparison of some morphological features and biometric data of Paralia species from Korean coastal waters
  • [Fig. 1.] How the Paralia valve characters were measured and taken using scanning electron microscopy. (A) Intercalary valve face view. Diameter (a), internal linking spines (thin arrow), outer marginal pores (thick arrow), inner marginal pores (arrowhead). (B) Separation valve face view. Diameter (a), internal linking spines (thin arrow), outer marginal pores (thick arrow), inner marginal pores (arrowhead). (C) Number of fenestrae (b), number of marginal linking spines (c). (D) Internal valve view. Number of striae (d), number of internal stria pores (e), rimoportula (thin arrow). Scale bars represent: A, 5 μm; B-D, 2 μm.
    How the Paralia valve characters were measured and taken using scanning electron microscopy. (A) Intercalary valve face view. Diameter (a), internal linking spines (thin arrow), outer marginal pores (thick arrow), inner marginal pores (arrowhead). (B) Separation valve face view. Diameter (a), internal linking spines (thin arrow), outer marginal pores (thick arrow), inner marginal pores (arrowhead). (C) Number of fenestrae (b), number of marginal linking spines (c). (D) Internal valve view. Number of striae (d), number of internal stria pores (e), rimoportula (thin arrow). Scale bars represent: A, 5 μm; B-D, 2 μm.
  • [Fig. 2.] Micrographs of Paralia fenestrata taken using light microscopy (A, C & E) and scanning electron microscopy (B, D & F-I). (A & B) Girdle view of four-celled chain. Upper (A) focus girdle view of the specimen. (C) Valve view of separation valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (D) Valve view of separation valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (E) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (F) Valve view of intercalary valve with interlocking radiating processes. Internal linking spines (thin arrow), marginal pore (thick arrow). (G) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal linking spines (thick arrow). Visible fenestra (dashed square), external pore of the rimoportula (arrowhead). (H) Girdle view of two cells. Each cell has marginal linking spines and copulae. Marginal linking spines (thin arrow) in relief valve, marginal linking spines (thick arrow) in intaglio valve, slits in copulae (arrowhead). (I) Internal valve view. Rimoportula (arrowheads). Scale bars represent: A & C-E, 10 μm; B, F & I, 5 μm; G, 2 μm; H, 1 μm.
    Micrographs of Paralia fenestrata taken using light microscopy (A, C & E) and scanning electron microscopy (B, D & F-I). (A & B) Girdle view of four-celled chain. Upper (A) focus girdle view of the specimen. (C) Valve view of separation valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (D) Valve view of separation valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (E) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (F) Valve view of intercalary valve with interlocking radiating processes. Internal linking spines (thin arrow), marginal pore (thick arrow). (G) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal linking spines (thick arrow). Visible fenestra (dashed square), external pore of the rimoportula (arrowhead). (H) Girdle view of two cells. Each cell has marginal linking spines and copulae. Marginal linking spines (thin arrow) in relief valve, marginal linking spines (thick arrow) in intaglio valve, slits in copulae (arrowhead). (I) Internal valve view. Rimoportula (arrowheads). Scale bars represent: A & C-E, 10 μm; B, F & I, 5 μm; G, 2 μm; H, 1 μm.
  • [Fig. 3.] Micrographs of Paralia guyana taken using light microscopy (A, B & E) and scanning electron microscopy (C, D & F-I). (A-C) Girdle view of eight-celled chain. Upper (A) and middle (B) focus girdle view of the specimen. (D) Girdle view of interlocked, sibling, separation valves with internal linking spines (thick arrow); slits in copulae (arrowhead) and well-developed prickles (thin arrow). (E) Valve view of separation valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (F) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (G) Valve view of intercalary valve with interlocking radiating processes and fenestrae. Internal linking spines (thin arrow), marginal pore (thick arrow). (H) Girdle view of interlocked, sibling, intercalary valves. Extended marginal linking spines (thin arrow) in relief valve; short, blunt marginal linking spines (thick arrow) in intaglio valve; visible fenestra (dashed square). (I) Internal valve view with internal striae and rimoportulae. Rimoportula (arrowheads). Scale bars represent: A-C & E, 10 μm; D & H, 5 μm; F & G, 2 μm; I, 1 μm.
    Micrographs of Paralia guyana taken using light microscopy (A, B & E) and scanning electron microscopy (C, D & F-I). (A-C) Girdle view of eight-celled chain. Upper (A) and middle (B) focus girdle view of the specimen. (D) Girdle view of interlocked, sibling, separation valves with internal linking spines (thick arrow); slits in copulae (arrowhead) and well-developed prickles (thin arrow). (E) Valve view of separation valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (F) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (G) Valve view of intercalary valve with interlocking radiating processes and fenestrae. Internal linking spines (thin arrow), marginal pore (thick arrow). (H) Girdle view of interlocked, sibling, intercalary valves. Extended marginal linking spines (thin arrow) in relief valve; short, blunt marginal linking spines (thick arrow) in intaglio valve; visible fenestra (dashed square). (I) Internal valve view with internal striae and rimoportulae. Rimoportula (arrowheads). Scale bars represent: A-C & E, 10 μm; D & H, 5 μm; F & G, 2 μm; I, 1 μm.
  • [FIG. 4.] Micrographs of Paralia marina taken using light microscopy (A, D & F) and scanning electron microscopy (B, C, E & G-I). (A & B) Girdle view of chained cells. Upper (A) focus girdle view of 11-celled chain. (C) Girdle view of interlocked, sibling, separation valves. Slits in copulae (arrowhead) and internal linking spines (thin arrow), decussated pattern of poroid areolae (dashed square). (D) Valve view of separation valve. Internal linking spines (thin arrow); marginal pore (thick arrow). (E) Valve view of separation valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (F) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (G) Valve view of intercalary valve with interlocking radiating processes. Internal linking spines (thin arrow); medium-sized marginal pore (thick arrow). (H) Sibling valves held together by long and capitate-shaped marginal linking spines. There are two rings of pores and fenestrae parallel to the mantle edge. Marginal linking spines (thin arrow) in relief valve; marginal linking spines (thick arrow) in intaglio valve; rimoportula (arrowhead); external pore of the rimoportula (dashed square). (I) Internal valve view with internal striae and rimoportulae. Rimoportula (arrowheads). Scale bars represent: A & F, 10 μm; B-D, 5 μm; E, 1 μm; G-I, 2 μm.
    Micrographs of Paralia marina taken using light microscopy (A, D & F) and scanning electron microscopy (B, C, E & G-I). (A & B) Girdle view of chained cells. Upper (A) focus girdle view of 11-celled chain. (C) Girdle view of interlocked, sibling, separation valves. Slits in copulae (arrowhead) and internal linking spines (thin arrow), decussated pattern of poroid areolae (dashed square). (D) Valve view of separation valve. Internal linking spines (thin arrow); marginal pore (thick arrow). (E) Valve view of separation valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (F) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (G) Valve view of intercalary valve with interlocking radiating processes. Internal linking spines (thin arrow); medium-sized marginal pore (thick arrow). (H) Sibling valves held together by long and capitate-shaped marginal linking spines. There are two rings of pores and fenestrae parallel to the mantle edge. Marginal linking spines (thin arrow) in relief valve; marginal linking spines (thick arrow) in intaglio valve; rimoportula (arrowhead); external pore of the rimoportula (dashed square). (I) Internal valve view with internal striae and rimoportulae. Rimoportula (arrowheads). Scale bars represent: A & F, 10 μm; B-D, 5 μm; E, 1 μm; G-I, 2 μm.
  • [Fig. 5.] Micrographs of Paralia cf. obscura taken using light microscopy (A, C & D) and scanning electron microscopy (B & E-G). (A & B) Girdle view of four-celled chain. Upper (A) focus girdle view of the specimens. (C) Valve view of separation valve. Irregular pattern of internal linking spines (thin arrow); marginal pore (thick arrow). (D) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (E) Valve view of intercalary valve with interlocking radiating processes. Internal linking spines (thin arrow), medium-sized marginal pore (thick arrow). (F) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (arrowhead), broken marginal linking spine (thick arrow), visible narrow fenestrae (dashed square). (G) Girdle view of two sibling valves showing the irregular spatulate shape of marginal linking spines and copulae. Marginal linking spines (thin arrow) in relief valve, marginal linking spines (thick arrow) in intaglio valve, slits in copulae (arrowhead). Scale bars represent: A, C & D, 10 μm; B & E, 5 μm; F, 2 μm; G, 1 μm.
    Micrographs of Paralia cf. obscura taken using light microscopy (A, C & D) and scanning electron microscopy (B & E-G). (A & B) Girdle view of four-celled chain. Upper (A) focus girdle view of the specimens. (C) Valve view of separation valve. Irregular pattern of internal linking spines (thin arrow); marginal pore (thick arrow). (D) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (E) Valve view of intercalary valve with interlocking radiating processes. Internal linking spines (thin arrow), medium-sized marginal pore (thick arrow). (F) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (arrowhead), broken marginal linking spine (thick arrow), visible narrow fenestrae (dashed square). (G) Girdle view of two sibling valves showing the irregular spatulate shape of marginal linking spines and copulae. Marginal linking spines (thin arrow) in relief valve, marginal linking spines (thick arrow) in intaglio valve, slits in copulae (arrowhead). Scale bars represent: A, C & D, 10 μm; B & E, 5 μm; F, 2 μm; G, 1 μm.
  • [Fig. 6.] Micrographs of Paralia sulcata taken using light microscopy (A, B, E & G) and scanning electron microscopy (C, D, F & H-J). (A-C) Girdle view of chained cells. Upper (A) and middle (B) focus girdle view of the specimen. (D) Girdle view of interlocked, sibling, separation valves. Wedgeshaped internal linking spines (thin arrow). (E) Valve view of separation valve. Irregular pattern of internal linking spines (thin arrow). (F) Valve view of separation valve. Irregular pattern of internal linking spines (thin arrow), marginal pore (thick arrow). (G) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (H) Valve view of intercalary valve with interlocking radiating processes. Internal linking spines (thin arrow), marginal pore (thick arrow). (I) Girdle view of intercalary valve. Slender, spatula, rounded tips of internal linking spines (thin arrow) in relief valve; flat tip of marginal linking spines (thick arrow) in intaglio valve; obscure fenestrae (dashed square); slits in copulae (arrowhead). (J) Internal valve view with internal striae and rimoportulae. Rimoportula (arrowheads). Scale bars represent: A, B, E & G, 10 μm; C, F, H & J, 5 μm; D, 2 μm; I, 1 μm.
    Micrographs of Paralia sulcata taken using light microscopy (A, B, E & G) and scanning electron microscopy (C, D, F & H-J). (A-C) Girdle view of chained cells. Upper (A) and middle (B) focus girdle view of the specimen. (D) Girdle view of interlocked, sibling, separation valves. Wedgeshaped internal linking spines (thin arrow). (E) Valve view of separation valve. Irregular pattern of internal linking spines (thin arrow). (F) Valve view of separation valve. Irregular pattern of internal linking spines (thin arrow), marginal pore (thick arrow). (G) Valve view of intercalary valve. Internal linking spines (thin arrow), marginal pore (thick arrow). (H) Valve view of intercalary valve with interlocking radiating processes. Internal linking spines (thin arrow), marginal pore (thick arrow). (I) Girdle view of intercalary valve. Slender, spatula, rounded tips of internal linking spines (thin arrow) in relief valve; flat tip of marginal linking spines (thick arrow) in intaglio valve; obscure fenestrae (dashed square); slits in copulae (arrowhead). (J) Internal valve view with internal striae and rimoportulae. Rimoportula (arrowheads). Scale bars represent: A, B, E & G, 10 μm; C, F, H & J, 5 μm; D, 2 μm; I, 1 μm.
  • [Fig. 7.] Non-metric multidimensional scaling analysis plot based on Bray Curtis similarities between Paralia species in this study and 5 species distinguished by CLUSTER analysis (symbols). Yellow symbols represent species in Paralia fenestrata, red symbols represent species in P. guyana, black symbols represent species in P. marina, green symbols represent species in P. cf. obscura, and blue symbols represent species in P. sulcata.
    Non-metric multidimensional scaling analysis plot based on Bray Curtis similarities between Paralia species in this study and 5 species distinguished by CLUSTER analysis (symbols). Yellow symbols represent species in Paralia fenestrata, red symbols represent species in P. guyana, black symbols represent species in P. marina, green symbols represent species in P. cf. obscura, and blue symbols represent species in P. sulcata.
  • [Table 2.] Comparison of ratio of Paralia species from Korean coastal waters
    Comparison of ratio of Paralia species from Korean coastal waters