Abstract
It has been accepted that we know less than 10% of the identified diversity in the marine microbial world and the diatoms are no exception. Even the species that we think we can easily recognize are often cryptic species, and even less is known of their life histories and spatial and temporal trends in their abundance and distribution. With new molecular and analytical techniques, we can advance our knowledge of a species to understand its morphological range, biogeographies and reproductive isolation. Moreover, some of molecular techniques are very sensitive. Depending on the species-level question(s) being asked, the molecular tools appropriate to answer them differ greatly.
Similar content being viewed by others
References
Abarca N, Jahn R, Zimmermann J, Enke N (2014) Does the cosmopolitan diatom Gomphonema parvulum (Kützing) Kützing have a biogeography? PLoS ONE 9:e86885. https://doi.org/10.1371/journal.pone.0086885
Amann R, Lin C, Key R, Montgomery L, Stahl DA (1992) Diversity among Fibrobacter isolates: towards a phylogenetic classification. Syst Appl Microbiol 15:23–31
Amato A, Montresor M (2008) Morphology, phylogeny, and sexual cycle of Pseudo-nitzschia mannii sp. nov. (Bacillariophyceae): a pseudo-cryptic species within the P. pseudodelicatissima complex. Phycologia 47:487–497
Amato A, Kooistra WHCF, Ghiron JHL, Mann DG, Proschold T, Montresor M (2007) Reproductive isolation among sympatric cryptic species in marine diatoms. Protist 158:193–207
Apothéloz-Perret-Gentil L, Cordonier A, Straud F, Iseli J, Esling P, Pawlowski J (2017) Taxonomy-free molecular diatom index for high-throughput eDNA biomonitoring. Mol Ecol Res. https://doi.org/10.1111/1755-0998.12668
Balzano S, Percopo I, Sianao R, Gourvil P, Chanoine M, Marie D, Vaulot D, Sarno D (2017) Morphological and genetic diversity of Beaufort Sea diatoms with high contributions from the Chaetoceros neogracilis species complex. J Phycol 53:161–187
Basu S, Pati S, Mapleson D, Russo MT, Vitale L, Fevola C, Maumus F, Casotti R, Mock T, Caccamo M, Montresor M, Sanges R, Ferrante MI (2017) Finding a partner in the ocean: molecular and evolutionary bases of the response to sexual cues in a planktonic diatom. New Phytol. https://doi.org/10.1111/nph.14557
Behnke A, Friedl T, Chepurnov V, Mann DG (2004) Reproductive compatibility and rDNA sequence analyses in the Sellaphora pupula species complex (Bacillariophyta). J Phycol 40:193–208
Bendif EM, Probert I, Diaz-Rosas F, van den Engh G, Young JR, von Dassow P (2014) Recent reticulate evolution in the ecologically dominant lineage of coccolithophores. Front Microbiol. https://doi.org/10.3389/fmicb.2016.00784
Bendif EM, Probert I, Young JR, von Dassow P (2015) Morphological and phylogenetic characterization of new Gephyrocapsa isolates suggests introgressive hybridization in the Emiliania/Gephyrocapsa complex (Haptophyta). Protist. https://doi.org/10.1016/j.protis.2015.05.003
Beszteri B, Acs E, Medlin LK (2005) Conventional and geometric morphometric studies of valve ultrastructural variation in two closely related Cyclotella species (Bacillariophyceae). Eur J Phycol 40:73–88
Beszteri B, John U, Medlin LK (2007) An assessment of cryptic genetic diversity within the Cyclotella meneghiniana species complex (Bacillariophyta) based on nuclear and plastid genes, and amplified fragment length polymorphisms. Eur J Phycol 42:47–60
Bowler C (2017) Tara oceans: eco-systems biology at planetary scale. Presentation at 7th applied phycology conference Nantes, June 2017
Casteleyn G, Chepurnov VA, Leliaert F, Mann DG, Bates SS, Lundholm N, Rhodes L, Sabbe K, Vyverman W (2008) Pseudo-nitzschia pungens (Bacillariophyceae): a cosmopolitan species? Harmful Algae 7:241–257
Coleman AW (2000) The significant of a coincidence between evolutionary landmarks in mating affinity and a DNA sequence. Protist 151:1–9
Coleman AW, Mai JC (1997) Ribosomal DNA ITS-1 and ITS-2 sequence comparisons as a tool for predicting genetic relatedness. J Mol Evol 44:258–271
Cox EJ (2009) What’s in a name? Diatom classification should reflect systematic relationships. Acta Bot Croat 68:443–454
Cox EJ (2014) Diatom identification in the face of changing species concepts and evidence of phenotypic plasticity. J Micropalaeontol. https://doi.org/10.1144/jmpaleo2014-014
Cracraft J (1989) Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and process of differentiation. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer Assoc, Sunderland, pp 28–59
Edgar RK, Saleh AI, Edgar SM (2015) A morphometric diagnosis using continuous characters of Pinnunavis edkuensis, sp. nov. (Bacillariophyta: Bacillariophyceae), a brackish-marine species from Egypt. Phytotaxa 212:1–56
Engesmo A, Eikrem W, Seoane S, Smith K, Edvardsen B, Hofgaard A, Tomas CR (2016) New insights into the morphology and phylogeny of Heterosigma akashiwo (Raphidophyceae), with the description of Heterosigma minor sp. nov. Phycologia 55:279–294
Evans KM, Wortley AH, Mann DG (2007) An assessment of potential diatom barcode genes (cox1 rbcL 18S, ITS rDNA) and their effectiveness in determining relationships in Sellaphora (Bacillariophyta). Protist 158:349–361
Evans KM, Wortley AH, Simpson GE, Chepurnov VA, Mann DG (2008) A molecular systematic approach to explore diversity within the Sellaphora pupula species complex. J Phycol 44:215–231
Evans KM, Chepurnov VA, Sluiman HJ, Thomas SJ, Spears BM, Mann DG (2009) Highly differentiated populations of the freshwater diatom Sellaphora capitata suggest limited dispersal and opportunities for allopatric speciation. Protist 160:386–396
Garrido-Cardenas JA, Garcia-Maroto F, Alvares-Bermej JA, Manznao-Agugliaro F (2017) DNA sequencing sensors: an overview. Sensors 17:588. https://doi.org/10.3390/s17030588
Goldman N, Paddock TBB, Shaw KM (1990) Quantitative analysis of shape variation in populations of Surirella fastuosa. Diatom Res 5:25–42
Gomez F, Wang L, Hernandez-Becerril DU, Lisunova Lopes RM, Lin S (2017) Molecular phylogeny suggests transfer of Hemidiscus into Actinocyclus (Coscinodiscales, Coscinodiscophyceae). Diatom Res 32:21–28
Gosling EM (1994) Speciation and species concepts in the marine environment. In: Beaumont AR (ed) Genetics and evolution of aquatic organisms. Chapmann Hall, London, pp 1–15
Hamsher SE, Evans KM, Mann DG, Poulickova A, Saunders GW (2011) Barcoding diatoms: exploring alternatives to COI-5P. Protist 162:405–422
Hasle GR, Medlin LK, Syvertsen EE (1994) Synedropsis gen. nov. a genus of araphid diatoms associated with sea ice. Phycologia 33:248–270
Hebert PDN, Cywinska A, Ball LS, DeWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond Ser B 270:313–321
Hillebrand H, Soininen J, Snoeijs P (2010) Warming leads to higher species turnover in a coastal ecosystem. Glob Change Biol. https://doi.org/10.1111/j.1365-2486.2009.02045.x
Huss VAR, Don R, Grossman U, Kessler E (1986) Deoxyribonucleic acid reassociation in the taxonomy of the genus Chlorella. Arch Microbiol 145:329–333
Huss VAR, Huss G, Kessler E (1989) Deoxyribonucleic acid reassociation and interspecies relationships of the genus Chlorella Chlorophyceae. Plant Syst Evol 168:1–82
Jahn R, Abarca N, Gemeinholzer B, Mora D, Skibbe O, Kulikovskiy M, Gusev E, Kusber W-H, Zimmermann J (2017) Planothidium lanceolatum and Planothidium frequentissimum reinvestigated with molecular methods and morphology: four new species and the taxonomic importance of the sinus and cavum. Diatom Res 32:75–107. https://doi.org/10.1080/0269249X.2017.1312548
John U, Litaker RW, Montresor M, Murray S, Brosnahan B, Anderson DM (2014) Formal revision of the Alexandrium tamarense species complex (Dinophyceae) taxonomy: the introduction of five species with emphasis on molecular-based (rDNA) classification. Protist 165:779–804
Kaczmarska I, Ehrman JM (2015) Auxosporulation in Paralia guyana MacGillivary (Bacillariophyta) and possible new insights into the habit of the earliest diatoms. PLoS ONE 10:e0141150. https://doi.org/10.1371/journal.pone.0141150
Kermarrec L, Franc A, Rimet F et al (2013) Next generation sequencing to inventory taxonomic diversity in eukaryotic communities: a test for freshwater diatoms. Mol Ecol Res 13:607–619
Kermarrec L, Franc A, Rimet F et al (2014) A Next generation sequencing approach to river monitoring using benthic diatoms. Fresh Sci 33:349–363
Kistenich S, Dreßler M, Zimmermann J, Hübener T, Bastrop HR, Jahn R (2014) An investigation into the morphology and genetics of Cyclotella comensis and closely related taxa. Diatom Res. https://doi.org/10.1080/0269249X.2014.922125
Kitching IJ, Forey PL, Humphries CJ, Williams DM (1998) Cladistics: the theory and practice of parsimony analysis, 2nd edn. Oxford University Press, Oxford, 229 pp
Klee R, Houk V (1996) Morphology and ultrastructure of Cyclotella woltereckii Hustedt (Bacillariophyceae). Arch Protist 147:19–27
Knowlton N (1993) Sibling species in the sea. Ann Rev Ecol Syst 24:189–216
Kooistra WHCF, Sarno D, Balzano S, Gu H, Andersen RA, Zingone A (2008) Global diversity and biogeography of Skeletonema species (Bacillariophyta). Protist 159:177–193
Kooistra WHCF, Sarno D, Hernandez-Becerril DU, Assmy P, Di Prisco C, Montresor M (2010) Comparative molecular and morphological phylogenetic analyses of taxa in the Chaetocerotaceae (Bacillariophyta). Phycologia 49:471–500
Lohbeck KT, Riebesell U, Thorsten BH, Reusch TBH (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nat Geosci 5:346–351
Luddington IA, Kaczmarska I, Lovejoy C (2012) Distance and character-based evaluation of the v4 region of the 18 s rRNA gene for the identification of diatoms (Bacillariophyceae). PLoS ONE 7:e45664. https://doi.org/10.1371/journal.pone.0045664
Malviya S, Scalcob E, Audicc S, Vincenta F, Veluchamya A, Poulaind J, Winckerd P, Iudiconeb D, de Vargas C, Bittnera L, Zingone A, Bowler C (2017) Insights into global diatom distribution and diversity in the world’s ocean. PNAS. https://doi.org/10.1073/pnas.1509523113
Manhart JR, McCourt RM (1992) Molecular data and species concepts in the algae. J Phycol 28:730–737
Mann DG (1999) The species concept in diatoms. Phycologia 38:437–495
Mann DG, Chepurnov VA, Droop SJM (1999) sexuality, incompatibility, size variation, and preferential polyandry in natural populations and clones of Sellaphora pupula (Bacillariophyceae). J Phycol 35:151–170
Mann DG, McDonald SM, Bayer MM, Droop SJM, Chepurnov VA, Loke RE, Ciobanu A, Du Buf JMH (2004) The Sellaphora pupula species complex (Bacillariophyceae): morphometric analysis, ultrastructure and mating data. Phycologia 43:459–482
Mann DG, Sato S, Trobajo R, Vanomelingen P, Souffreau C (2010) DNA barcoding for species identification and discovery in diatoms. Cryptogam Algol 31:557–577
Medlin LK (1997) Can molecular techniques help define species limits? Diatom 13:19–23
Medlin LK (2008) Molecular clocks and inferring evolutionary milestones and biogeography in the microalgae. In: Okada H, Mawatari SF, Suzuki N, Gautam P (eds) Proceedings of International Symposium “The Origin and Evolution of Natural diversity”, 1–5 October 2007, Sapporo, pp 31–42
Medlin LK (2014) Evolution of the diatoms: VIII. Re-examination of the SSU-rRNA gene using multiple outgroups and a cladistic analysis of valve features. J Biodivers Biopros Dev 1:129. https://doi.org/10.4172/2376-0214.1000129
Medlin LK (2016a) Opinion: can coalescent models explain deep divergences in the diatoms and argue for the acceptance of paraphyletic taxa at all taxonomic hierarchies? Nova Hedwig. https://doi.org/10.1127/nova_hedwigia/2015/0295
Medlin LK (2016b) A timescale for diatom evolution based on four molecular markers: reassessment of ghost lineages and major steps defining diatom evolution. Vie et Milleu 65:219–238
Medlin LK, Fryxell GA (1984) Structure, life history and systematics of Rhoicosphenia (Bacillariophyta). IV. Changes in frustule morphology concomitant with size reduction in Rhoicosphenia genuflexa (Kütz.) Medlin. J Phycol 20:101–108
Medlin LK, Kooistra WHCF (2010) Methods to estimate the diversity in the marine photosynthetic protist community with illustrations from case studies: a review. Biol Divers Assess Mol Methods 2:973–1014
Medlin LK, Elwood HJ, Stickel S, Sogin ML (1991) Morphological and genetic variation within the diatom Skeletonema costatum Bacillariophyta: evidence for a new species Skeletonema pseudocostatum. J Phycol 27:514–524
Medlin LK, Lange M, Baumann MEM (1994) Genetic differentiation among three colony-forming species of Phaeocystis: further evidence for the phylogeny of the Prymnesiophyta. Phycologia 33:199–212
Medlin LK, Barker GLA, Campbell L, Green JC, Hayes PK, Marie D, Wrieden S, Vaulot D (1996) Genetic characterisation of Emiliania huxleyi (Haptophyta). J Mar Syst 9:13–31
Medlin LK, Sato S, Mann DG, Kooistra WCHF (2008) Molecular evidence confirms sister relationship of Ardissonea, Climacosphenia, and Toxarium within the bipolar centric diatoms (Bacillariophyta, Mediophyceae), and cladistic analyses confirm that extremely elongated shape has arisen twice in the diatoms. J Phycol 44:1340–1348
Mizuno M (2006) Evolution of meiotic patterns of oogenesis and spermatogenesis in centric diatoms. Phycol Res 54:57–64
Mizuno M (2008) Evolution of centric diatoms inferred from patterns of oogenesis and spermatogenesis. Phycol Res 56:156–165
Moniz MBJ, Kaczmarska I (2009) Barcoding diatoms: is there a good marker? Mol Ecol Res 9:65–74
Moniz MBJ, Kaczmarska I (2010) Barcoding of diatoms: nuclear encoded ITS revisited. Protist 161:7–34
Nanjappa D, Kooistra WHCF, Zingone A (2013) A reappraisal of the genus Leptocylindrus (Bacillariophyta), with the addition of three species and the erection of Tenuicylindrus gen. nov. J Phycol 49:917–936
Nanjappa D, Audic S, Romac S, Kooistra WCHF, Zingone A (2014) Assessment of species diversity and distribution of an ancient diatom lineage using a DNA metabarcoding approach. PLoS ONE 9:e103810
Pawlowski J, Audic S, Adl S, Bass D, Belbahri L et al (2012) CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biol 10:e1001419. https://doi.org/10.1371/journal.pbio.1001419
Pennesi C, Poulin M, Totti C (2016) Phylogenetic relationships and biogeography of the diatom genus Mastogloia (Bacillariophyceae): revision of the Section Ellipticae including the description of new taxa. Protist 167:148–173
Pinseel E, Hejdukova E, Vanormelingen P, Kopalova K, Vyverman W, Van de Vijver B (2017a) Pinnularia catenaborealis sp. nov. (Bacillariophyceae), a unique chain-forming diatom species from James Ross Island and Vega Island (Maritime Antarctica). Phycologia 56:94–107
Pinseel E, Vanormelingen P, Hamilton P, Vyverman W, Van de Vijver B, Kopalova K (2017b) Molecular and morphological characterization of the Achnanthidium minutissimum complex (Bacillariophyta) in Petuniabukta (Spitsbergen, High Arctic) including the description of A. digitatum sp. nov. Eur J Phycol. https://doi.org/10.1080/09670262.2017.1283540
Pinseel E, Vanormelingen P, Janssens S et al (2017c) Opening Pandora’s box: a diatom species complex as a case study for the diversity and biogeography of terrestrial micro-eukaryotes. Abstracts from the 11th international phycological congress. Phycologia 56:146 (supplement 4)
Piredda R, Sarno D, Lange CB, Tomasino MP, Zingonne A, Montresor M (2017) Diatom resting stages in surface sediments: a pilot study comparing next generation sequencing and serial dilution cultures. Cryptogam Algol 38:31–46
Rappé MS, Kemp PF, Giovannoni SJ (1995) Chromophyte plastid 16S ribosomal RNA genes found in a clone library from Atlantic Ocean Seawater. J Phycol 31:979–988
Rimet F, Trobajo R, Mann DG, Kermarrec L, Franc A, Domaizon I, Bouchez A (2014) When is sampling complete? The effects of geographical range and marker choice on perceived diversity in Nitzschia palea (Bacillariophyta). Protist 165:245–259
Rose DL, Cox EJ (2013) Some diatom species do not show a gradual decrease in cell size as they reproduce. Fundam Appl Limnol 182:117–122
Rose DL, Cox EJ (2014) What constitutes Gomphonema parvulum? Long-term culture studies show that some varieties of G. parvulum belong with other Gomphonema. Plant Ecol Evol 147:366–373
Rovira L, Trobajo R, Sato S, Ibanez C, Mann DG (2015) Genetic and physiological diversity in the diatom Nitzschia inconspicua. J Euk Microbiol 62:815–832
Ruggerior MV, Barra L, Kooistra WHCF, Zingone A (2015) Diversity and temporal pattern of Pseudo-nitzschia species (Bacillariophyceae) through the molecular lens. Harmful Algae. https://doi.org/10.1016/j.hal.2014.12.001
Rynearson TA, Armbrust EV (2005) Maintenance of clonal diversity during a spring bloom of the centric diatom Ditylum brightwellii. Mol Ecol 14:1631–1640
Rynearson TA, Lin EO, Armbrust EV (2009) Metapopulation structure in the planktonic diatom Ditylum brightwellii (Bacillariophyceae). Protist 160:111–121
Sarno D, Kooistra WHCF, Medlin LK, Percopo I, Zingone A (2005) Diversity in the genus Skeletonema (Bacillariophyceae): Skeletonema costatum (Bacillariophyceae) consists of several genetically and morphologically distinct species with the description of four new species. J Phycol 41:151–176
Souffreau C, Verbruggen H, Wolfe AP, Vanormelingen P, Siver PA, Cox EJ, Mann DG, Van de Vijver B, Sabbe S, Vyverman W (2011) A time-calibrated multi-gene phylogeny of the diatom genus Pinnularia. Mol Syst Evol 61:866–879
Sournia A (1988) Phaeocystis Prymnesiophyceae: how many species? Nova Hedwig 47:211–217
Subirana L, Péquin B, Michely S, Escand M-L, Meillanda J, Derelle E, Marine B, Piganeau G, Desdevises Y, Moreau H, Nigel H, Grimsley NH (2013) Morphology, genome plasticity, and phylogeny in the genus Ostreococcus reveal a cryptic species, O. mediterraneus sp. nov. (Mamiellales, Mamiellophyceae). Protist 164:643–659
Theriot EC, Ashworth M, Nakov T, Ruck E, Jansen RK (2015) Dissecting signal and noise in diatom chloroplast protein encoding genes with phylogenetic information profiling. Mol Phylo Evol 89:28–36
Trobajo R, Clavero E, Chepurnov VA, Koen Kabbe, Mann DG, Ishihara S, Cox EJ (2009) Morphological, genetic and mating diversity within the widespread bioindicator Nitzschia palea (Bacillariophyceae). Phycologia 48:443–459
Trobajo R, Mann DG, Clavero E, Evans KM, Vanormelingen P, McGregor RC (2010) The use of partial cox1, rbcL and LSU rDNA sequences for phylogenetics and species identification within the Nitzschia palea species complex (Bacillariophyceae). Eur J Phycol 45:413–425
Urbánková P, Scharfen V, Kulichová J (2016) Molecular and automated identification of the diatom genus Frustulia in northern Europe. Diatom Res 31:217–229. https://doi.org/10.1080/0269249X.2016.1224780
Vanderlaan TA, Ebach MC, Williams DM, Wilkins JS (2013) Defining and redefining monophyly: Haeckel, Hennig, Ashlock, Nelson and the proliferation of definitions. Aust Syst Bot 26:347–355
Vanormelingen P, Chepurnov VA, Mann DG, Cousin S, Vyverman W (2007) Congruence of morphological, reproductive and ITS rDNA sequence data in some Australasian Eunotia bilunaris (Bacillariophyta). Eur J Phycol 42:61–79
Vanormelingen P, Chepurnov VA, Mann DG, Sabbe K, Vyverman W (2008) Genetic divergence and reproductive barriers among morphologically heterogeneous sympatric isolates of Eunotia bilunaris sensu lato (Bacillariophyta). Protist 159:73–90
Vanormelingen P, Evans KM, Chepurnov VA, Vyverman W, Mann DG (2013) Molecular species discovery in the diatom Sellaphora and its congruence with mating trials. Fottea 13:133–148
Vanormelingen P, Evans KM, Mann DG, Lance SL, Debeer AE, D’Hondt S, Verstraete T, de Meester L, Vyverman W (2015) Genotypic diversity and differentiation among populations of two benthic freshwater diatoms as revealed by microsatellites. Mol Ecol. https://doi.org/10.1111/mec.13336
Vaulot D, Birrien J-L, Marie D, Casotti R, Veldhuis MJW, Kraay GW, Chretiennot-Dinet M-J (1994) Morphology, ploidy, pigment composition and genome size of cultured strains of Phaeocysts. J Phycol 30:1022–1035
Wetzel CE, Ector L, Van de Vijver B, Compère P, Mann DG (2015) Morphology, typification and critical analysis of some ecologically important small naviculoid species (Bacillariophyta). Fottea Olomouc 15:203–234
Whitaker K, Rynearson TA (2017) Evidence for environmental and ecological selection in a microbe with no geographic limits to gene flow. PNAS. https://doi.org/10.1073/pnas.1612346114
Williams DM (2007) Classification and diatom systematics: the past, the present and the future. In: Brodie J, Lewis J (eds) Unravelling the algae—the past, present and future of algal systematics. CRC Press, Baton Rouge, pp 57–91
Woodard K, Kulichová J, Poláčková T, Neustupa J (2016) Morphometric allometry of representatives of three naviculoid genera throughout their life cycle. Diatom Res 31:231–242. https://doi.org/10.1080/0269249X.2016.1227375
Young JR, Liu H, Probert I, Aris-Brosou S, De Vargas C (2014) Morphospecies versus phylospecies concepts for evaluating phytoplankton diversity: the case of the coccolithophores. Cryptogam Algol 35:353–377
Zimmermann J, Jahn R, Gemeinholzer B (2011) Barcoding diatoms: evaluation of the V4 sub-region on the 18S rRNA gene, including new primers and protocols. Org Divers Evol. https://doi.org/10.1007/s13127-011-0050-6
Zimmermann J, Glöckner G, Jahn R, Enke N, Gemeinholzer B (2014a) Metabarcoding vs morphological identication to assess diatom diversity in environmental studies. Mol Ecol Res. https://doi.org/10.1111/1755-0998.12336
Zimmermann J, Abarca N, Enk N, Skibbe O, Kusber W-H et al (2014b) Taxonomic reference libraries for environmental barcoding: a best practice example from diatom research. PLoS ONE 9:e108793. https://doi.org/10.1371/journal.pone.0108793
Zingone A, Percopo I, Sims PA, Sarno D (2005) Diversity in the genus Skeletonema (Bacillariophyceae). I. A re-examination of the type material of Skeletonema costatum, with the description of S. grevillei sp. nov. J Phycol 41:140–150
Acknowledgements
Dr. D. G. Mann critically read my manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Medlin, L.K. Mini review: Diatom species as seen through a molecular window. Braz. J. Bot 41, 457–469 (2018). https://doi.org/10.1007/s40415-018-0444-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-018-0444-1