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Biological flora of Central Europe: Marsilea quadrifolia L

https://doi.org/10.1016/j.ppees.2021.125641Get rights and content

Highlights

  • Marsilea quadrifolia is a rare Eurasian aquatic fern species.

  • It is characterized by heterospory, an ancestral trait that evolved in the first seeds.

  • It is a flagship species, being listed in Directive 92/43/CEE and Bern Convention.

  • It is threatened by human activities producing loss of quality and habitat destruction.

  • In Asia it is used as a food source and in traditional Ayurvedic medicine.

Abstract

Marsilea quadrifolia L. is a leptosporangiate aquatic fern which has a played key role in the evolutionary history of plants. It is characterized by heterospory, the ancestral progressive trait that led to the evolution of seeds. The species has creeping, fleshy, adventitious roots containing multiple rhizomes. From the rhizomes a four-leaf clover grows above the water level with a long petiole, at the base of which the sporocarps containing spores are located. Its life cycle is characterized by alternation of generations; reproduction occurs either sexually or by vegetative propagation. The species grows in wet habitats containing shallow water. In the natural environment this includes lakes and small rivers; in agricultural areas it can be found in ditches and rice fields. The species can tolerate nutrient rich waters and because of its phytoremediation properties is capable of partially counteracting the negative effects induced by a moderate organic enrichment of sediments. It has been harvested for centuries in Asian countries as both a food source and for ethnobotanical use in Ayurvedic medicine. Supposed medicinal properties include antibacterial, diuretic, depurative, cytotoxic and antioxidant effects, but these require further investigation and testing.

M. quadrifolia has a widespread distribution, occurring throughout central-southern Europe and extending from Eurasia to tropical and temperate areas of eastern Asia and North America, where it is considered a non-native species. Despite its wide distribution, in its home range the species is threatened with extinction and has already been locally extirpated in several European countries. As a result, it is listed as “Vulnerable” in the European Union Red List due to its scattered distribution and declining population. Habitat loss and degradation, excessive water eutrophication, and agricultural practices such as the use of herbicides, mechanization and simplified rotation are the main threats to the species.

As it is listed in Appendix I of the Bern Convention and in Annexes II and IV of Directive 92/43/EEC as a strictly protected species, in situ and ex situ conservation activities have been conducted in most European countries. Reintroduction, cultivation in botanical gardens and in vitro propagation are the most commonly applied conservation methods.

Section snippets

Taxonomy and evolution

Systematic position: Pteridophyta

Division. Pteridophyta

Class. Polypodiopsida

Order. Salviniales (Marsileales)

Family. Marsileaceae

Genus. Marsilea

Species. Marsilea quadrifolia L.

Marsilea quadrifolia L. Sp. Pl. 2: 1099 (1753), commonly named European water clover but also four-leaf clover, water shamrock and pepperwort, is an aquatic fern with creeping, fleshy, adventitious roots containing multiple rhizomes (Benson et al., 2004, Fig. 1). The species owes its name to Carl Linnaeus (1753) who named

Life cycle

The life cycle of M. quadrifolia is characterized by the alternation of generations, i.e. alternate succession of haploid gametophyte and diploid sporophyte (Johnson, 1986). More often, however, vegetative propagation through the division of rhizomes occurs.

Reproduction and development

Vegetative propagation occurs by means of rhizomes.

Sexual reproduction takes place via sporocarps and the release of micro- and megaspores (Schneider and Pryer, 2002, Fig. 1B). Gametophyte generation is completed within 24 h, and the first

Previous and current distribution

M. quadrifolia has a widespread global distribution: it is native to Eurasia and considered an alien species in North America (Benson et al., 2004). Populations have been reported in the following countries and regions (Strat, 2012; Hassler, 2020): Afghanistan, Albania, Austria, Azerbaijan, Bangladesh, Bhutan, Bosnia and Herzegovina, Bulgaria, Cambodia, Canada, China, Croatia, France, Georgia, Germany, Greece, Hungary, India, Iran, Italy, Japan, Kazakhstan, Malaysia, Moldova, Montenegro,

Ethnobotanical uses

M. quadrifolia has been harvested for centuries for its ethnobotanical importance and as a source of food (Ripa et al., 2009). In India, it has been used in the local Ayurvedic medicine by the Vaidyas (people who practice Ayurveda) for thousands of years (Joy et al., 2019). In particular, it is used by the Indian tribal communities of Kadars, Pulaiyars, Malasars, Malaimalasars, Anamailais hills, and Western Ghats (Ramachandran, 2007). Here, the plant is called Sunishannaka and references can be

Threats

M. quadrifolia is mainly threatened by human activities that result in habitat loss and degradation. Drainage of wetlands, management changes of fishponds, and agriculture intensification or abandonment are responsible for its population decline throughout Europe (Dehondt et al., 2005). Water eutrophication and pollution, and changes in agricultural practices such as the application of herbicides, are responsible for the species extirpation in Spain (Moreno, 2008), and the cause of a strong

Inspirations for further research

Several experimental studies have already been conducted in M. quadrifolia, including morphological, ecophysiological and medicinal studies. However, to gain further insight into M. quadrifolia conservation needs, it may be appropriate to focus on the secondary habitat of the species, i.e., rice paddies. In this context, information is lacking within the communities where M. quadrifolia grows, such as the relationship with other invasive weeds as well as with rice. Indeed, even though it has

Funding

The Grant of Excellence Departments, MIUR-Italy (ARTICOLO 1, COMMI 314–337 LEGGE 232/2016) is gratefully acknowledged for the support to one of the authors (Prof. Thomas Abeli).

Declaration of Competing Interest

The authors report no declarations of interest.

Acknowledgments

The authors are grateful to Dr. A. Efremov (Omsk State Pedagogical University, Russia) for implementing data on species distribution in Asia. We would like to thank Fiona Jane White (University of Pavia) for revising the English.

References (125)

  • A.C. Albrecht

    Identification guide to Nordic aphids associated with mosses, horsetails and ferns (Bryophyta, Equisetophyta, Polypodiophyta) (Insecta, Hemiptera, Aphidoidea)

    Eur. J. Taxon.

    (2015)
  • G. Ashwini et al.

    Pharmacological evaluation of Marsilea quadrifolia plant extracts against Alzheimer’s disease

    Int. J. Drug Dev. Res.

    (2012)
  • D. Ballesteros et al.

    Fern conservation: spore, gametophyte, and sporophyte ex situ storage, in vitro culture, and cryopreservation

  • Z. Barina et al.

    Vörös Lista

  • R.M. Bateman et al.

    Heterospory: the most iterative key innovation in the evolution of plants

    Biol. Rev.

    (1994)
  • A.M. Bendre et al.
  • A.J. Benson et al.

    Summary Report of Nonindigenous Aquatic Species in U.S. Fish and Wildlife Service Region 5

    (2004)
  • R. Bercu

    Anatomical features of the vegetative organs of Marsilea quadrifolia L

    Contrib. Bot.

    (2004)
  • BGCI

    Botanic Gardens Conservation International PlantSerch Tool

    (2020)
  • S. Bhadra et al.

    Cholinesterase inhibition activity of Marsilea quadrifolia Linn. An edible leafy vegetable from West Bengal, India

    Nat. Prod. Res.

    (2012)
  • M. Bilz et al.

    European Red List of Vascular Plants

    (2011)
  • R. Bolpagni et al.

    Sediment nutrient drivers of the growth dynamics of the rare fern Marsilea quadrifolia

    Hydrobiologia

    (2017)
  • A. Braun

    Hr. Braun theilte neuere Untersuchungen über die Gattungen Marsilea und Pilularia

    (1871)
  • A. Carapeto et al.

    Lista Vermelha da Flora Vascular de Portugal Continental

    (2020)
  • M.E. Collinson

    Diversification of modern heterosporous pteridophytes

  • A. Corli et al.

    Coexistence of rice production and threatened plant species: testing Marsilea quadrifolia L. In N-Italy

    Paddy Water Environ

    (2021)
  • F. Dehondt et al.

    Connaissance de la flore rare ou menacée de Franche-Comté, Marsilea quadrifolia L

    (2005)
  • A. Dewanji et al.

    Chemical composition of two semi-aquatic plants for food use

    Plant Foods Hum. Nutr.

    (1993)
  • G. Duca et al.

    Cartea roşie a Republicii Moldova

    (2015)
  • S. Đug et al.

    Knjiga 2 – Crvena Lista Flore Federacije Bosne I Hercegovine

    (2013)
  • Environment Agency of Japan
    (2000)
  • E. Estrelles et al.

    Recuperación y reintroducción de Marsilea quadrifolia en los arrozales del Delta del Ebro (Tarragona, España)

    Bot. Complut.

    (2001)
  • E. Estrelles et al.

    Situación de las poblaciones valencianas del género Marsilea: medidas para su conservación

    Bot. Complut.

    (2001)
  • European Environmental Agency

    Eunis Biodiversity Database, Marsilea quadrifolia L

    (2020)
  • V. Feráková et al.
  • E. Ferrarini et al.

    Iconographia palynologica pteridophytorum italiae

    Webbia

    (1986)
  • M. García Criado et al.

    European Red List of Lycopods and Ferns

    (2017)
  • GBIF

    Marsilea quadrifolia L

    (2020)
  • R. Gentili et al.

    Marsilea quadrifolia L., in: Schede per una Lista Rossa della Flora vascolare e crittogamica Italiana

    Inf. Bot. Ital.

    (2010)
  • K. Gopalakrishnan et al.

    Antimicrobial activity of Marsilea quadrifolia (L.) against some selected pathogenic microorganisms

    Br. Microbiol. Res. J.

    (2014)
  • K. Gopalakrishnan et al.

    Phytochemical content of leaf and stem of Marsilea quadrifolia (L.)

    J Plant Sci Phytopathol.

    (2017)
  • K.M. Gupta

    Marsilea. Botanical Monograph No. 2

    (1962)
  • A.K. Gupta

    Marsilea quadrifolia

    The IUCN Red List of Threatened Species 2011

    (2011)
  • L. Hanson et al.

    DNA amounts for five pteridophyte species fill phylogenetic gaps in C-value data

    Bot. J. Linn. Soc.

    (2002)
  • M. Hassler

    world ferns: checklist of ferns and lycophytes of the world

  • L. Holm et al.

    World Weeds: Natural Histories and Distribution

    (1997)
  • S. Husák et al.

    Contribution to the ecology of Marsilea quadrifolia l

    Folia Geobot Phytotx.

    (1986)
  • N. Hussain et al.

    Transformation of a highly pernicious and toxic weed parthenium into an eco- friendly organic fertilizer by vermicomposting

    Int. J. Environ. Res.

    (2016)
  • A. Ibars et al.

    Recent developments in ex situ and in situ conservation of ferns

    Fern Gaz.

    (2012)
  • D. Ivanova et al.

    Marsilea quadrifolia L.

  • Cited by (0)

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