New insights into the phylogeny and relationships within the worldwide genus Riccardia (Aneuraceae, Marchantiophytina)

Lucile Rabeau, S. Robbert Gradstein, Jean-Yves Dubuisson, Martin Nebel, Dietmar Quandt, Catherine Reeb


With 280 accepted species, the genus Riccardia S.F.Gray (Aneuraceae) is one of the most speciose genera of simple thalloid liverworts. The current classification of this genus is based on morphological and limited-sampling molecular studies. Very few molecular data are available and a comprehensive view of evolutionary relationships within the genus is still lacking. A phylogeny focusing on relationships within the large genus Riccardia has not been conducted. Here we propose the first worldwide molecular phylogeny of the genus Riccardia, based on Bayesian inference and parsimony ratchet analyses of sequences from three plastid regions (psbA-trnH, rps4, trnL-F). The results support the monophyly of Riccardia and a new monospecific genus, Afroriccardia Reeb & Gradst. gen. nov., is described based on molecular and morphological evidence. The results indicate that several currently recognized infrageneric divisions and a few species are not monophyletic, suggesting that further analyses are needed to arrive at a proper understanding of the phylogeny of the genus. Although evidence for an Andean clade was found, most of the species appear scattered in different clades without clear geographical segregation. Broader sampling and further analyses are necessary in order to improve our understanding of the phylogeny of this poorly known liverwort genus.


Afroriccardia gen. nov.; Aneuraceae; liverworts; phylogeny; Riccardia

Full Text:




Aranda S.C., Gradstein S.R., Patiño J., Laenen B., Désamoré A. & Vanderpoorten A. 2014. Phylogeny, classification and species delimitation in the liverwort genus Odontoschisma (Cephaloziaceae). Taxon 63: 1008–1025.

Arnell S. 1952. South African species of Riccardia. Botaniska Notiser 2: 139–156.

Arnell S. 1963. Hepaticae of South Africa. Swedish Natural Science Research Council, Stockholm.

Berrie G.K. 1966. Polyploidy in some West African species of Riccardia (Gray). Revue Bryologique et Lichénologique 34: 302–308.

Bidartondo M.I. & Duckett J.G. 2010. Conservative ecological and evolutionary patterns in liverwort-fungal symbioses. Proceedings of the Royal Society B 277: 485–492.

Borsch T. & Quandt D. 2009. Mutational dynamics and phylogenetic utility of non-coding plastid DNA. Plant Systematics and Evolution 282: 169–199.

Bremer K. 1985. Summary of green plant phylogeny and classification. Cladistics 1: 369–385.

Brown E.A. & Braggins J. 1989. A revision of the genus Riccardia S.F. Gray in New Zealand with notes on the genus Aneura Dum. Journal of the Hattori Botanical Laboratory 66: 1–32.

Carter B.E. 2012. Species delimitation and cryptic diversity in the moss genus Scleropodium (Brachytheciaceae). Molecular Phylogenetics and Evolution 63: 891–903.

Chalaud G. 1930. Les derniers stades de la spermatogénèse chez les hépatiques. Annales Bryologici 3: 41–50.

Chen S., Yao H., Han J., Liu C., Song J., Shi L., Zhu Y., Ma X., Gao T., Pang X., Luo K., Li Y., Li X., Jia X., Lin Y. & Leon C. 2010. Validation of the ITS2 region as a novel DNA barcode for identifying medicinal plant species. PLoS ONE 5(1): e8613.

Crandall-Stotler B.J., Forrest L. & Stotler R.E. 2005. Evolutionary trends in the simple thalloid liverworts (Marchantiophyta, Jungermanniopsida subclass Metzgeriidae). Taxon 54: 299–316.

Crandall-Stotler B., Stotler R.E. & Long D. 2009. Phylogeny and classification of the Marchantiophyta. Edinburgh Journal of Botany 66: 155–198.

Davis E.C. 2004. A molecular phylogeny of leafy liverworts (Marchantiophyta). Monographs in Systematic Botany from the Missouri Botanical Garden 98: 87–118.

Doweld A. 2001. Prosyllabus Tracheophytorum: Tentamen Systematis Plantarum Vascularium (Tracheophyta). Geos, Moscow.

Fontaneto D., Flot J.F. & Cuong Q.T. 2015. Guidelines for DNA taxonomy, with a focus on the meiofauna. Marine Biodiversity 45(3): 433–451.

Forrest L.L. & Crandall-Stotler B.J. 2004. A phylogeny of the simple thalloid liverworts (Jungermanniopsida, Metzgeriidae) as inferred from five chloroplast genes. Monographs in Systematic Botany from the Missouri Botanical Garden 98: 119–140.

Forrest L.L. & Crandall-Stotler B.J. 2005. Progress towards a robust phylogeny for the liverworts, with a particular focus on the simple thalloids. Journal of the Hattori Botanical Laboratory 97: 127–159.

Forrest L.L., Davis E.C., Long D.G., Crandall-Stotler B.J., Clark A. & Hollingsworth M.L. 2006. Unraveling the evolutionary history of the liverworts (Marchantiophyta): multiple taxa, genomes and analyses. The Bryologist 109: 303–334.[303:UTEHOT]2.0.CO;2

Furuki T. 1991. A taxonomical revision of the Aneuraceae (Hepaticae) of Japan. Journal of the Hattori Botanical Laboratory 70: 293–397.

Furuki T. 1994. Taxonomic studies of Asiatic species of Aneuraceae (Hepaticae). III. Riccardia subgen. Thornoneura Furuki. Hikobia 11: 463–467.

Furuki T. 1995. Taxonomic studies of Asiatic species of Aneuraceae (Hepaticae). II. Riccardia subgen. Hyaloneura Schust. Journal of the Hattori Botanical Laboratory 78: 111–118.

Furuki T. & Tan B.C. 2013. Taxonomical studies of the family Aneuraceae (Marchantiophyta) of Singapore. Natural History Research 12: 71–79.

Gradstein S.R. 2001. Liverworts and hornworts: keys and descriptions. Memoirs of the New York Botanical Garden 86: 70–239.

Gradstein S.R. 2011. Guide to the Liverworts and Hornworts of Java. Seameo Biotrop, Bogor, Indonesia.

Gradstein S.R. 2013. Afro-American hepatics revisited. Polish Botanical Journal 58: 149–177.

Gradstein S.R. & Costa D. 2003. The liverworts and hornworts of Brazil. Memoirs of the New York Botanical Garden 87: 1–318.

Grolle R. & Long D.G. 2000. An annotated checklist of the Hepaticae and Anthocerotae of Europe and Macaronesia. Journal of Bryology 22: 101–140.

Hässel de Menendez G.G. 1972. Revisión taxonómica del género “Riccardia” (Hepaticae). Especies patagónicas y subantarcticas incluyendo las Islas Juan Fernández, Malvinas y Georgia del Sur. Revista del Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” e Instituto Nacional de Investigación de las Ciencias Naturales: Ciencias Botánicas 4: 1–242.

Hedenäs L., Desamoré A., Laenen B., Papp B., Quandt D., Gonzáles-Macebo J.M., Patiño J., Vanderpoorten A. & Stech M. 2014. Three species for the price of one with the moss Homalothecium sericeum s.l. Taxon 63: 249–257.

Heinrichs J., Feldberg K., Scheben A., Czumaj A., Pócs T., Schneider H. & Schäfer-Verwimp A. 2015. Integrative taxonomy of Lepidolejeunea (Porellales, Jungermanniopsida): ocelli allow the recognition of two neglected species. Taxon 64: 216–228.

He-Nygrén X., Juslén A., Ahonen I., Glenny D. & Piippo S. 2006. Illuminating the evolutionary history of liverworts (Marchantiophyta) - towards a natural classification. Cladistics 22: 1–31.

Hewson H.J. 1970. The family Aneuraceae in Australia and New Guinea: the genus Aneura. Proceedings of the Linnean Society of New South Wales 94: 173–193. Available from [accessed 10 Dec. 2016].

Huelsenbeck J.P., Ronquist F., Nielsen R. & Bollback J.P. 2001. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294: 2310–2314.

Hutsemékers V., Vieira C.C., Ros R.M., Huttunen S. & Vanderpoorten A. 2012. Morphology informed by phylogeny reveals unexpected patterns of species differentiation in the aquatic moss Rhynchostegium riparioides s.l. Molecular Phylogeny and Evolution 62: 748–755.

Jones E.W. 1956. African Hepatics: XI. The genus Riccardia in Tropical Africa. Transactions of the British Bryological Society 3: 74–84.

Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., Thierer T., Ashton B., Mentjies P. & Drummond A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.

Kelchner S.A. 2000. The evolution of non-coding chloroplast DNA and its application in plant systematics. Annals of the Missouri Botanical Garden 87: 482–498.

Klinggräff H.E.M. 1858. Die Höheren Cryptogamen Preussens, 11. Koch, Königsberg.

Kottke I., Beiter A., Weiss M., Haug I., Oberwinkler F., Nebel M. 2003. Heterobasidiomycetes form symbiotic associations with hepatics: Jungermanniales have sebacinoid mycobionts while Aneura pinguis (Metzgeriales) is associated with a Tulasnella species. Mycological Research 107: 957–968.

Krause C., Garnica S., Bauer R., Nebel M. 2011. Aneuraceae (Metzgeriales) and tulasnelloid fungi (Basidiomycota) - a model for early steps in fungal symbiosis. Fungal Biology 115: 839–851.

Lanfear R., Calcott B., Ho W.S.Y.W. & Guindon S. 2012. PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29 (6): 1695–1701.

Lang A.S., Bocksberger G. & Stech M. 2015. Phylogeny and species delimitations in European Dicranum (Dicranaceae, Bryophyta) inferred from nuclear and plastid DNA. Molecular Phylogenetics and Evolution 92: 217–225.

Liu Y., Yan H.F., Cao T. & Ge X. 2010. Evaluation of 10 plant barcodes in Bryophyta (Mosses). Journal of Systematics and Evolution 48: 36–46.

Meenks J. 1987. Studies on Colombian cryptogams. XXVIII. A guide to tropical Andean species of Riccardia. Journal of the Hattori Botanical Laboratory 62: 161–182.

Meenks J. & Pócs T. 1985. East African bryophytes. IX. Aneuraceae. Abstracta Botanica 9: 79–98.

Miller M.A., Pfeiffer W. & Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans: 1–8.

Mizutani M. & Hattori S. 1957. An etude on the systematics of Japanese Riccardias. Journal of the Hattori Botanical Laboratory 18: 27–64.

Müller K. 2007. PRAP2 – Parsimony and likelihood ratchet analyses with PAUP, v. 0.9. Available from [accessed 27 Jan. 2017]

Müller K., Quandt D., Müller J. & Neinhuis C. 2010. PhyDE® 0.997: Phylogenetic Data Editor. Available from [accessed 8 Dec. 2016]

Nadot S., Bajon R. & LeJeune B. 1994. The chloroplast gene rps4 as a tool for the study of Poaceae phylogeny. Plant Systematics and Evolution 191: 27–38.

Nebel M. 2016. Aneuraceae. In: Söderström L., Hagborg A., von Konrat M., Bartholomew-Began S., Bell D., Briscoe L., Brown E., Cargill D.C., Costa D.P., Crandall-Stotler B.J., Cooper E.D., Dauphin G., Engel J.J., Feldberg K., Glenny D., Gradstein S.R., He X., Heinrichs J., Hentschel J., Ilkiu-Borges A.L., Katagiri T., Konstantinova N.A., Larrain J., Long D.G., Nebel M., Pócs T., Felisa Puche F., Reiner-Drehwald E., Renner M.A.M., Sass-Gyarmati A., Schäfer-Verwimp A., Segarra-Moragues J.G., Stotler R.E., Sukkharak P., Thiers B.M., Uribe J., Vaňa J., Villarreal J.C., Wigginton M., Zhang L. & Zhu R.-L. (eds) World Checklist of Hornworts and Liverworts. PhytoKeys 59: 435–456.

Nixon K.C. 1999. The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15: 407–414.

Paton J.A. 1999. The Liverwort Flora of the British Isles. Harley Books, Colchester, U.K.

Perold S.M. 2001a. Studies in the liverwort family Aneuraceae (Metzgeriales) from southern Africa. 1. The genus Aneura and its local representative. Bothalia 31: 167–173.

Perold S.M. 2001b. Studies in the liverwort family Aneuraceae (Metzgeriales) from southern Africa. 2. The genus Riccardia and its type species, R. multifida, with confirmation of its presence in the region. Bothalia 31: 183–187.

Perold S.M. 2002a. Studies in the liverwort family Aneuraceae (Metzgeriales) from northern Africa. 3. Riccardia compacta. Bothalia 32: 15–19.

Perold S.M. 2002b. Studies in the liverwort family Aneuraceae (Metzgeriales) from northern Africa. 4. Riccardia obtusa. Bothalia 32: 181–184.

Perold S.M. 2003. Studies in the liverwort family Aneuraceae (Metzgeriales) from northern Africa. 5. Riccardia amazonica. Bothalia 33: 99–104.

Preuβing M., Olsson S., Schäfer-Verwimp A., Wickett N.J., Wicke S., Quandt D. & Nebel M. 2010. New insights in the evolution of the liverwort family Aneuraceae (Metzgeriales, Marchantiophyta), with emphasis on the genus Lobatiriccardia. Taxon 59: 1424–1440.

Puillandre N., Lambert A., Brouillet S. & Achaz G. 2012. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21: 1864–1877.

Qiu Y.L. & Palmer J.D. 1999. Phylogeny of early land plants: insights from genes and genomes. Trends in Plant Science 4: 26–30.

Quandt D. & Stech M. 2004. Molecular evolution of the trnT-trnF region in bryophytes. Plant Biology 6: 545–554.

Quandt D. & Stech M. 2005. Molecular evolution of the trnLUAA intron in bryophytes. Molecular Phylogenetics and Evolution 36: 429–443.

Quandt, D. Müller K. & Huttunen S. 2003. Characterisation of the chloroplast DNA psbT-H region and the influence of dyad symmetrical elements on phylogenetic reconstructions. Plant Biology 5: 400–410.

Rambaut A., Suchard M.A., Xie D. & Drummond A.J. 2014. Tracer v. 1.6. Available from [accessed 8 Dec. 2016]

Reeb C. & Bardat J. 2014. Studies on African Riccardia types and related material. Cryptogamie, Bryologie 35: 47–75.

Rico G. 2011. Methods for cell clearing and rehydration in thalloid liverworts. Tropical Bryology 33: 12–18.

Ruggiero M.A., Gordon D.P., Orrell T.M., Bailly N., Bourgoin T., Brusca R.C., Cavalier-Smith T., Guiry M.D. & Kirk P.M. 2015. A higher level classification of all living organisms. PLoS ONE 10: e0119248.

Sang T., Crawford D. & Stuessy T. 1997. Chloroplast DNA phylogeny, reticulate evolution, and biogeography of Paeonia (Paeoniaceae). American Journal of Botany 84: 1120–1136.

Schäfer-Verwimp A., Lehnert M. & Nebel M. 2013. Contribution to the knowledge of the bryophyte flora of Ecuador. Phytotaxa 128 (1): 1–63.

Schuster R.M. 1985. Austral Hepaticae, XIX. Some taxa new to New Zealand and New Caledonia. Phytologia 56: 449–464. Available from [accessed 10 Dec. 2016]

Schuster R.M. 1989. Studies on the hepatic flora of the Prince Edward Islands. I: Aneuraceae. Journal of the Hattori Botanical Laboratory 67: 59–108.

Schuster R.M. 1992. The Hepaticae and Anthocerotae of North America. Volume VI. Field Museum of Natural History, Chicago.

Souza-Chies T.T, Bittar G., Nadot S., Carter L., Besin E. & LeJeune B. 1997. Phylogenetic analysis of Iridaceae with parsimony and distance methods using the plastid gene rps4. Plant Systematics and Evolution 204: 109–123.

Stech M. & Quandt D. 2010. 20,000 species and five key markers: the status of molecular bryophyte phylogenetics. Phytotaxa 9: 196–228.

Stephani F. 1890. Hepaticae Africanae novae in insulis Bourbon, Maurice et Madagascar lectae. Botanical Gazette 15 (11): 281–292.

Stotler R. & Crandall-Stotler B. 1977. A checklist of the liverworts and hornworts of North America. The Bryologist 80: 405–428.

Sukkharak P., Gradstein S.R. & Stech M. 2011. Phylogeny, taxon circumscriptions, and character evolution in the core Ptychanthoideae (Lejeuneaceae, Marchantiophyta). Taxon 60: 1607–1622.

Swofford D.L. 2002. PAUP*: Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.

Taberlet P., Gielly L., Pautou G. & Bouvet J. 1991. Universal primers for amplification of 3 noncoding regions of chloroplast DNA. Plant Molecular Biology 17: 1105–1109.

Tamura K., Peterson D., Peterson N., Stecher G., Nei M. & Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.

Thiers B. Continuously updated. Index Herbariorum: A global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Available from [accessed 8 Dec. 2016].

Van Zanten B.O. & Gradstein S.R. 1988. Experimental dispersal geography of neotropical liverworts. Beihefte zur Nova Hedwigia 90: 41–94.

Wicke S., Schneeweiss G.M., dePamphilis C.W., Müller K.F. & Quandt D. 2011. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Molecular Biology 76: 273–297.

Wickett N.J. & Goffinet B. 2008. Origin and relationships of the myc-heterotrophic liverwort Cryptothallus mirabilis Malmb. (Metzgeriales, Marchantiophyta). Botanical Journal of the Linnean Society 156: 1–12.

Wigginton M.J. (ed.) 2004. EW Jones‘s Liverwort and Hornwort Flora of West Africa. National Botanic Garden, Meise, Belgium.

Zhang J., Kapli P., Pavlidis P. & Stamatakis A. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876.


  • There are currently no refbacks.

License URL:








Credits for header's photographs