Azolla#Reproduction

Phylogeny of Azolla{{cite journal |last1=Nitta |first1=Joel H. |last2=Schuettpelz |first2=Eric |last3=Ramírez-Barahona |first3=Santiago |last4=Iwasaki |first4=Wataru |display-authors=et al. |year=2022 |title=An Open and Continuously Updated Fern Tree of Life |journal=Frontiers in Plant Science |volume=13 |issue= |page= 909768| doi=10.3389/fpls.2022.909768 |pmid= 36092417|pmc= 9449725|bibcode= 2022FrPS...1309768N|doi-access=free}}{{cite web|last1= |first1= |last2= |display-authors=et al. |year=2023 |title=Tree viewer: interactive visualization of FTOL |url=https://fernphy.github.io/viewer.html |version=FTOL v1.4.0 [GenBank release 253] |access-date=8 March 2023}}

{{Clade | style=font-size:100%;line-height:80%

|label1=Azolla

|1={{clade

|1=A. nilotica Decne. ex Mett. (Nile Azolla)

|2={{clade

|1={{clade

|1=A. filiculoides Lam. (Large mosquito fern)

|2=A. rubra R.Br.

}}

|2={{clade

|1=A. caroliniana Willdenow 1810 (Eastern/Carolinian mosquito fern)

|2={{clade

|1=Azolla cristata Kaulf. (Mexican mosquito fern)

|2=A. pinnata R.Br. (Ferny/Pacific Azolla; Feathered mosquitofern)

}}

}}

}}

}}

}}

Other species include:{{cite journal |last1=Evrard |first1=C. |last2=Van Hove |first2=C. |title=Taxonomy of the American Azolla species (Azollaceae): A critical review |journal=Systematics and Geography of Plants |date=2004 |volume=74 |pages=301–318}}{{cite web |url=http://www.tropicos.org/NameSubordinateTaxa.aspx?nameid=40023609 |title=Name - Azolla Lam. subordinate taxa |work=Tropicos |publisher=Missouri Botanical Garden |location=Saint Louis, Missouri |access-date=February 19, 2010}}{{cite web |url=http://www.ipni.org:80/ipni/advPlantNameSearch.do?find_genus=Azolla&find_rankToReturn=spec&output_format=normal&query_type=by_query&back_page=plantsearch |title=Query Results for Genus Azolla |work=IPNI |access-date=February 19, 2010}}{{cite web |url=http://www.nobanis.org/files/factsheets/Azolla_filiculoides.pdf |title=NOBANIS -- Invasive Alien Species Fact Sheet -- Azolla filiculoides |author=Hussner, A. |location=Heinrich Heine Universität, Düsseldorf |year=2006 |work=Online Database of the North European and Baltic Network on Invasive Alien Species |access-date=February 19, 2010}}

At least six extinct species are known from the fossil record:

• Azolla intertrappea Sahni & H.S. Rao, 1934 (Eocene, India){{cite journal |last1=Arnold |first1=C.A. |year=1955 |title=A Tertiary Azolla from British Columbia |journal=Contributions from the Museum of. Paleontology, University of Michigan |volume=12 |issue=4 |pages=37–45 |url=http://deepblue.lib.umich.edu/bitstream/2027.42/48289/2/ID129.pdf}}
• Azolla berryi Brown, 1934 (Eocene, Green River Formation, Wyoming)
• Azolla prisca Chandler & Reid, 1926 (Oligocene, London Clay, Isle of Wight)
• Azolla tertiaria Berry, 1927 (Pliocene, Esmeralda Formation, Nevada)
• Azolla primaeva (Penhallow) Arnold, 1955 (Eocene, Allenby Formation, British Columbia)
• Azolla boliviensis Vajda & McLoughlin, 2005 (Maastrichtian – Paleocene, Eslaboacuten Formation and Flora Formation Bolivia){{cite journal |last1=Vajda |first1=V |author2=McLoughlin, S. |year=2005 |title=A new Maastrichtian-Paleocene Azolla species from Bolivia, with a comparison of the global record of coeval Azolla microfossils |journal=Alcheringa: An Australasian Journal of Palaeontology |volume=29 |issue=2 |pages=305–329 |doi=10.1080/03115510508619308 |bibcode=2005Alch...29..305V |s2cid=128643041}}

File:Azolla-13.3348RGB.tif

File:Canning rv azolla 10 gnangarra.jpg]]

Azolla is a highly productive plant that can double its biomass in 1.9 days,{{cite journal |journal=Aquatic Botany |volume=15 |issue=2 |pages=175–185 |date=1983 |title=The growth of four species of Azolla as affected by temperature |author=Iwao Watanabe, Nilda S.Berja |doi=10.1016/0304-3770(83)90027-X|bibcode=1983AqBot..15..175W }} depending on growing conditions. The plant can yield can reach 8–10 tonnes fresh matter per hectare in Asian paddy fields. 37.8 tonnes fresh weight/ha (2.78 t/ha dry weight) has been reported for A. pinnata in India.{{cite web |title=Hasan, M. R.; Chakrabarti, R., 2009. Use of algae and aquatic macrophytes as feed in small-scale aquaculture: A review. FAO Fisheries and Aquaculture technical paper, 531. FAO, Rome, Italy |url=https://www.fao.org/3/i1141e/i1141e00.htm |website=fao.org/ |access-date=18 August 2014}}

Azolla floats on the surface of water by means of numerous small, closely overlapping scale-like leaves, with their roots hanging in the water. They form a symbiotic relationship with the cyanobacterium Anabaena azollae,{{refn|1=Currently [https://lpsn.dsmz.de/species/trichormus-azollae Trichormus azollae] {{au|(Strasburger 1884) Komárek and Anagnostidis 1989}}. Synonyms: Nostoc azollae {{au|Strasburger 1883}}, Anabaena azollae {{au|Strasburger 1884}}, Desikacharya azollae {{au|(Strasburger 1884) Saraf et al. 2019}}.{{cn|date=January 2025}}|group=note}} which lives outside the cells of its host and which fixes atmospheric nitrogen.{{cite journal | pmc=2900214 | year=2010 | last1=Ran | first1=L. | last2=Larsson | first2=J. | last3=Vigil-Stenman | first3=T. | last4=Nylander | first4=J. A. | last5=Ininbergs | first5=K. | last6=Zheng | first6=W. W. | last7=Lapidus | first7=A. | last8=Lowry | first8=S. | last9=Haselkorn | first9=R. | last10=Bergman | first10=B. | title=Genome Erosion in a Nitrogen-Fixing Vertically Transmitted Endosymbiotic Multicellular Cyanobacterium | journal=PLOS ONE | volume=5 | issue=7 | pages=e11486 | doi=10.1371/journal.pone.0011486 | pmid=20628610 | bibcode=2010PLoSO...511486R | doi-access=free }} The typical limiting factor on its growth is phosphorus; thus, an abundance of phosphorus—due for example to eutrophication or chemical runoff—often leads to Azolla blooms. Unlike all other known plants, its symbiotic microorganism transfers directly from one generation to the next. A. azollae is completely dependent on its host, as several of its genes have either been lost or transferred to the nucleus in Azolla's cells.{{Cite web|url=https://www.geolsoc.org.uk/Geoscientist/Archive/June-2014/The-Arctic-Azolla-event|title=The Geological Society of London - The Arctic Azolla event|website=www.geolsoc.org.uk|date=April 8, 2025 }}

The nitrogen-fixing capability of Azolla has led to widespread use as a biofertiliser, especially in parts of southeast Asia. The plant has been used to bolster agricultural productivity in China for over a thousand years. When rice paddies are flooded in the spring, they can be planted with Azolla, which then quickly multiplies to cover the water, suppressing weeds. The rotting plant material resulting from the die-off of this Azolla releases nitrogen into the water for the rice plants, providing up to nine tonnes of protein per hectare per year.{{Cite web|url=http://www.fao.org/ag/AGA/AGAP/FRG/afris/DATA/558.htm|title=FAO figures}}

Azolla are weeds in many parts of the world, entirely covering some bodies of water. The myth that no mosquito can penetrate the coating of fern to lay its eggs in the water gives the plant its common name "mosquito fern";{{cite web |url=http://www.americaswetlandresources.com/wildlife_ecology/plants_animals_ecology/plants/mosquitofern.html |title=Mosquito Fern |access-date=2007-11-10 |work=America's Wetland Resource Center |publisher=Loyola University, New Orleans |archive-date=May 16, 2006 |archive-url=https://web.archive.org/web/20060516014940/http://www.americaswetlandresources.com/wildlife_ecology/plants_animals_ecology/plants/mosquitofern.html |url-status=dead }} however, Azolla may deter the survival of some of mosquito larvae.

Most species can produce large amounts of deoxyanthocyanins in response to various stresses,{{cite journal |doi=10.1007/BF02857915 |last1=Wagner |first1=G.M. |year=1997 |title=Azolla: a review of its biology and utilization |journal=Bot. Rev. |volume=63 |issue=1 |pages=1–26 |bibcode=1997BotRv..63....1W |s2cid=347780}} including bright sunlight and extreme temperatures,{{cite journal |doi=10.1007/BF02859886 |last1=Moore |first1=A. W. |year=1969 |title=Azolla: Biology and agronomic significance |journal=Bot. Rev. |volume=35 |issue=1 |pages=17–35 |bibcode=1969BotRv..35...17M |s2cid=42431293}}{{cite journal |last1=Zimmerman |first1=William J. |year=1985 |title=Biomass and Pigment Production in Three Isolates of Azolla II. Response to Light and Temperature Stress |journal=Ann. Bot. |volume=56 |issue=5 |pages=701–709 |doi=10.1093/oxfordjournals.aob.a087059}} causing the water surface to appear to be covered with an intensely red carpet. Herbivore feeding induces accumulation of deoxyanthocyanins and leads to a reduction in the proportion of polyunsaturated fatty acids in the fronds, thus lowering their palatability and nutritive value.{{cite journal |doi=10.1016/S0304-3770(02)00077-3 |last1=Cohen |first1=M.F. |last2=Meziane |first2=T. |last3=Tsuchiya |first3=M. |last4=Yamasaki |first4=H. |year=2002 |title=Feeding deterrence of Azolla in relation to deoxyanthocyanin and fatty acid composition |url=http://www.bashanfoundation.org/michael/michaelfeeding.pdf |journal=Aquatic Botany |volume=74 |issue=2 |pages=181–187 |bibcode=2002AqBot..74..181C |access-date=2010-01-22 |archive-url=https://web.archive.org/web/20081122000150/http://www.bashanfoundation.org/michael/michaelfeeding.pdf |archive-date=2008-11-22 |url-status=dead}}

Azolla cannot survive winters with prolonged freezing, so is often grown as an ornamental plant at high latitudes where it cannot establish itself firmly enough to become a weed. It is also not tolerant of salinity; normal plants cannot survive in greater than 1–1.6‰, and even conditioned organisms die if grown in water with a salinity above 5.5‰.{{cite journal

|author=Brinkhuis, H.

|author2=Schouten, S.|author3=Collinson, M.E.|author4=Sluijs, A.|author5=Sinninghe Damsté, J.S.|author6=Dickens, G.R.|author7=Huber, M.|author8=Cronin, T.M.|author9=Onodera, J.|author10=Takahashi, K.

|year=2006

|title=Episodic fresh surface waters in the Eocene Arctic Ocean

|journal=Nature

|volume=441

|pages=606–9

|url=http://www.nature.com/search/executeSearch?sp-q-9=NATURE&sp-q=Episodic+fresh+surface+waters+in+the+Eocene+Arctic+Ocean&sp-c=10&sp-x-9=cat&sp-s=date&submit=go&sp-a=sp1001702d&sp-sfvl-field=subject%7Cujournal&sp-x-1=ujournal&sp-p-1=phrase&sp-p=all

|access-date=2007-10-17

|doi=10.1038/nature04692

|pmid=16752440

|issue=7093

|bibcode=2006Natur.441..606B|display-authors=etal|hdl=11250/174278|s2cid=4412107|hdl-access=free}}

Azolla filiculoides (red azolla) is the only member of the family Azollaceae found in Tasmania, where it is a common native aquatic plant. It is often found behind farm dams and other still waterbodies. The plants are small (usually only a few cm across) and float, but they are fast growing, and can be abundant and form large mats. The plants are typically red, and have small, water repellent leaves.

{{more citations needed section|date=January 2025}}

File:Azolla megaspore Postglacial Galapagos Islands TEM longitudinal section 1.jpg

Azolla reproduces sexually, and asexually by splitting.

Like all ferns, sexual reproduction leads to spore formation, but unlike other members of this group, Azolla is heterosporous, producing spores of two kinds. During the summer months, numerous spherical structures called sporocarps form on the undersides of the branches. The male sporocarp is greenish or reddish and looks like the egg mass of an insect or spider. It is two millimeters in diameter, and bears numerous male sporangia. Male spores (microspores) are extremely small and are produced inside each microsporangium. Microspores tend to adhere in clumps called massulae.

Female sporocarps are much smaller, containing one sporangium and one functional spore. Since an individual female spore is considerably larger than a male spore, it is termed a megaspore.

Azolla has microscopic male and female gametophytes that develop inside the male and female spores. The female gametophyte protrudes from the megaspore and bears a small number of archegonia, each containing a single egg. The microspore forms a male gametophyte with a single antheridium which produces eight swimming sperm.{{cite book |author1=Scagel, Robert F. |author2=Bandoni, Robert J. |author3=Rouse, Glenn E. |author4=Schofield, W.B. |author5=Stein, Janet R. |author6=Taylor, T.M. |year=1965 |title=An Evolutionary Survey of the Plant Kingdom |place=Belmont, California |publisher=Wadsworth Publishing}} 658 pp. The barbed glochidia on the male spore clusters cause them to cling to the female megaspores, thus facilitating fertilization.

In addition to its traditional cultivation as a bio-fertilizer for wetland paddies, Azolla is finding increasing use for sustainable production of livestock feed.{{cite magazine |author1=Pillai, P. Kamalasanana |author2=Premalatha, S. |author3=Rajamony, S. |title=Azolla – a sustainable feed substitute for livestock |magazine=Farming Matters magazine |department=Small animals in focus |series=Azolla livestock feed |url=http://www.agriculturesnetwork.org/magazines/global/small-animals-in-focus/azolla-livestock-feed |access-date=2008-01-14}} Azolla is rich in protein, essential amino acids, vitamins, and minerals. Studies describe feeding Azolla to dairy cattle, pigs, ducks, and chickens, with reported increases in milk production, weight of broiler chickens and egg production of layers, as compared to conventional feed. One FAO study describes how Azolla integrates into a tropical biomass agricultural system, reducing the need for food supplements.{{cite journal |author1=Preston, T.R. |author2=Murgueitio, E. |year=1992–1993 |title=Sustainable intensive livestock systems for the humid tropics |journal=World Animal Review |series=Sustainable animal production |volume=71 |issn=1014-6954 |publisher=UN FAO |url=http://www.fao.org/docrep/u7600t/u7600T04.htm |access-date=2011-09-28}}

Concerns about biomagnification exist because the plant may contain the neurotoxin BMAA that remains present in the bodies of animals consuming it, and BMAA has been documented as passing along the food chain.{{cite journal |author1=Banack, S.A. |author2=Cox, P.A. |year=2003 |title=Biomagnification of cycad neurotoxins in flying foxes: Implications for ALS-PDC in Guam |journal=Neurology |volume=61 |issue=3 |pages=387–389 |doi=10.1212/01.wnl.0000078320.18564.9f |pmid=12913204 |s2cid=38943437}} Azolla may contain this substance that is a possible cause of neurodegenerative diseases, including causing ALS, Alzheimer's, and Parkinson's.{{cite web |author=Sjodin, Erik |date=December 2014 |title=Azolla, BMAA, and neurodegenerative diseases |url=https://www.academia.edu/10074317 |access-date=2015-01-08}}{{cite magazine |title=Are toxins in seafood causing ALS, Alzheimer's, and Parkinson's? |date=May 2011 |magazine=Discover Magazine |url=http://discovermagazine.com/2011/may/22-seafood-toxins-causing-als-alzheimers-parkinsons |access-date=2019-09-13}}{{cite news |author=Williams, Amy Bennett |date=7 August 2019 |title=Documentary about algae and public health debuts to sold-out crowd |newspaper=Fort Myers News-Press |url=https://www.news-press.com/story/tech/science/environment/2019/08/07/documentary-algae-and-public-health-debuts-sold-out-crowd/1926083001/}} Azolla has been suggested as a foodstuff for human consumption; however, no long-term studies of the safety of eating Azolla have been made on humans.{{cite book |last=Sjodin |first=Erik |year=2012 |title=The Azolla Cooking and Cultivation Project |publisher=Erik Sjödin |isbn=978-91-980686-0-3}} Previous studies attributed neurotoxin production to Anabaena flos-aquae species, which is also a type of nitrogen-fixing cyanobacteria.{{cite journal |last=Agnihotri |first=Vijai K. |year=2014 |title=Anabaena flos-aquae |journal=Critical Reviews in Environmental Science and Technology |volume=44 |issue=18 |pages=1995–2037 |s2cid=84472933 |doi=10.1080/10643389.2013.803797|bibcode=2014CREST..44.1995A }} Studies published in 2024 have found that “the Azolla–Nostoc azollae superorganism does not contain BMAA or their isomers DAB and AEG and that Azolla and N. azollae do not synthesize other common cyanotoxins.” {{cite journal |last=Bujak |first=Jonathan P. |year=2024 |title=Azolla as a Safe Food: Suppression of Cyanotoxin-Related Genes and Cyanotoxin Production in Its Symbiont, Nostoc azollae |journal=Plants |volume=13 |issue=19 |page=2707 | doi=10.3390/plants13192707 |doi-access=free |pmid=39409577 |pmc=11479175 |bibcode=2024Plnts..13.2707B }} Further research may be needed to ascertain whether A. azollae is a healthy foodstuff for humans.

Azolla has been used for at least one thousand years in rice paddies as a companion plant, to fix nitrogen and to block out light to prevent competition from other plants. Rice is planted when tall enough to poke through the Azolla layer. Mats of mature Azolla can also be used as a weed-suppressing mulch.

Rice farmers used Azolla as a rice biofertilizer 1500 years ago. The earliest known written record of this practice is in a book written by Jia Ssu Hsieh (Jia Si Xue) in 540 AD on The Art of Feeding the People (Chih Min Tao Shu). By the end of the Ming dynasty in the early 17th century, Azolla's use as a green compost was documented in local records.{{cite web |title=The East discovers Azolla |url=http://theazollafoundation.org/azolla/azollas-use-in-the-east/ |website=Azolla Foundation |access-date=18 August 2014}}

The myth that no mosquito can penetrate the coating of fern to lay its eggs in the water gives the plant its common name "mosquito fern". Azolla have been used to control mosquito larvae in rice fields. The plant grows in a thick mat on the surface of the water, making it more difficult for the larvae to reach the surface to breathe, effectively choking the larvae.{{cite journal |last1=Myer |first1=Landon |last2=Okech |first2=Bernard A. |last3=Mwobobia |first3=Isaac K. |last4=Kamau |first4=Anthony |last5=Muiruri |first5=Samuel |last6=Mutiso |first6=Noah |last7=Nyambura |first7=Joyce |last8=Mwatele |first8=Cassian |last9=Amano |first9=Teruaki |title=Use of Integrated Malaria Management Reduces Malaria in Kenya |journal=PLOS ONE |volume=3 |pages=e4050 |year=2008 |doi=10.1371/journal.pone.0004050 |editor1-last=Myer |editor1-first=Landon |issue=12 |pmid=19115000 |pmc=2603594 |bibcode=2008PLoSO...3.4050O |doi-access=free}}

Azolla has been proposed as a carbon sequestration modality. The proposal draws upon the hypothesized Azolla event that asserts that 55 million years ago, Azolla covered the Arctic – at the time a hot, tropical, freshwater environment – and then sank, permanently sequestering teratons of carbon that would otherwise have contributed to the planet's greenhouse effect. This ended a warming event that reached {{Convert|12-15|C-change|0}} warmer than present-day averages, eventually causing the formation of ice sheets in Antarctica and the current "icehouse period".{{cite web |last=Wang |first=Brian |title=Fix Hothouse Earth Just Like Last Time {{!}} NextBigFuture.com|url=https://www.nextbigfuture.com/2021/08/fix-hothouse-earth-just-like-last-time.html|access-date=2021-08-14|language=en-US}}{{cite web |date=2018-07-11 |title=Can a tiny fern help fight climate change and cut fertilizer use? |url=https://e360.yale.edu/digest/can-a-tiny-fern-help-fight-climate-change-and-cut-fertilizer-use-azolla |access-date=2021-11-25 |website=Yale E360 |language=en-US}}

They contribute significantly to decreasing the atmospheric CO₂ levels.

This fern has been introduced to other parts of the world, including the United Kingdom, where it has become a pest in some areas. A nominally tropical plant, it has adapted to the colder climate. It can form mats up to {{convert|30|cm}} thick and cover 100% of a water surface, preventing local insects and amphibians from reaching the surface.{{Cite web|url=https://insideecology.com/2017/11/01/invasive-non-native-species-uk-water-fern/|title=Invasive non-native species (UK) – Water fern|date=November 1, 2017|website=Inside Ecology}}

Azolla filiculoides is especially invasive because it has the ability to survive temperatures as low as {{convert|-22|C}} and can survive thin layers of ice built up on its growth. A. filiculoides spreads at rapid pace by way of Fragmentation which takes place in the rhizome (root-system). It can double its surface area and/or density in approximately 7-10 days under ideal conditions.

A. filiculoides disrupts aquatic ecosystems by altering abiotic conditions in the water. It can displace native plants in places where it is invasive, such as the duckweed Lemna minor in Poland. It is difficult to control due to its ability to reestablish itself from spores.

{{See also|Bioremediation}}

Azolla can remove chromium, nickel, copper, zinc, and lead from effluent. It can also remove lead from solutions containing 1–1000 ppm.{{cite book |title=Bioremediation Technologies: Principles and Practice |author1=Robert L. Irvine |author2=Subhas K. Sikdar |page=102 |url=https://books.google.com/books?id=oLNtgk_VKXsC&q=Bioremediation+of+gypsum&pg=PA81 |isbn=978-1-56676-561-9 |date=1998-01-08|publisher=CRC Press }}

==Notes==

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{{commons}}

• [http://theazollafoundation.org/ The Azolla Foundation] website
• [https://web.archive.org/web/20160308121032/http://www.azollaphilippines.com/home.html Azolla Philippines] website
• [https://web.archive.org/web/20100314135728/http://waynesword.palomar.edu/plnov98.htm Marriage Between A Fern & Cyanobacterium] by W.P. Armstrong

{{Plant classification}}

{{Fern classification}}

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Category:Aquatic plants

Category:Extant Maastrichtian first appearances

Category:Fern genera

Category:Invasive plant species in Japan

Category:Klondike Mountain Formation

Category:Maastrichtian genus first appearances

Category:Nitrogen-fixing crops

Category:Salviniales

Category:Taxa named by Jean-Baptiste Lamarck