Azolla

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Azolla
Temporal range: Maastrichtian-Holocene
Azolla caroliniana0.jpg
Azolla caroliniana
Scientific classification OOjs UI icon edit-ltr.svg
Kingdom: Plantae
Clade: Tracheophytes
Division: Polypodiophyta
Class: Polypodiopsida
Order: Salviniales
Family: Salviniaceae
Genus: Azolla
Lam. [1]
Type species
Azolla filiculoides [1]
Species

See text

Synonyms
  • CarpanthusRafinesque
  • RhizospermaMeyen

Azolla (mosquito fern, water fern, fairy moss) is a genus of seven species of aquatic ferns in the family Salviniaceae. They are extremely reduced in form and specialized, looking nothing like other typical ferns but more resembling the form of some mosses or even duckweeds. Azolla filiculoides is one of just two fern species for which a reference genome has been published. [2] It is believed that this genus grew so prolifically during the Eocene (and thus absorbed such a large amount of carbon) that it triggered a global cooling event that has lasted to the present. [3]

Contents

Azolla taken from the Philippines Azolla Plant.jpg
Azolla taken from the Philippines

Azolla may establish as an invasive plant in areas where it is not native [ where? ]. In such a situation it can alter aquatic ecosystems and biodiversity substantially. [4]

Phylogeny

Phylogeny of Azolla [5] [6]

Azolla

A. nilotica Decne. ex Mett. (Nile Azolla)

A. filiculoides Lam. (Large mosquito fern)

A. rubra R.Br.

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

Azolla cristata Kaulf. (Mexican mosquito fern)

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

Other species include: [7] [8] [9] [10]

Drawing of Azolla filiculoides, about 5 mm. Upper green leaves perform photosynthesis, lower lack chlorophyll. Azolla filiculoides drawing.png
Drawing of Azolla filiculoides, about 5 mm. Upper green leaves perform photosynthesis, lower lack chlorophyll.

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

Ecology

Azolla filiculoides root cross section Azolla-13.3348RGB.tif
Azolla filiculoides root cross section
Azolla covering the Canning River, Western Australia Canning rv azolla 10 gnangarra.jpg
Azolla covering the Canning River, Western Australia
Azolla on the Canning River, Western Australia Canning rv azolla 02 gnangarra.jpg
Azolla on the Canning River, Western Australia

Azolla is a highly productive plant. It can double its biomass in as little as 1.9 days, [13] depending on growing conditions, and yield can reach 8–10 tonnes fresh matter/ha in Asian rice fields. 37.8 t fresh weight/ha (2.78 t/ha dry weight) has been reported for Azolla pinnata in India (Hasan et al., 2009). [14]

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 , [a] an extracellular endosymbiont (living outside the host's cells) which fixes atmospheric nitrogen. [15] 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. [16]

SEM image of Azolla surface Azolla01.jpg
SEM image of Azolla surface

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. [17]

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", [18] and may deter the survival of some of the larvae.

Most species can produce large amounts of deoxyanthocyanins in response to various stresses, [19] including bright sunlight and extreme temperatures, [20] [21] 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. [22]

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‰. [23] [3]

Azolla filiculoides

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.

Reproduction

Scanning electron micrograph of a megaspore of the genus Azolla with adhering massulae from postal sediments of Laguna El Junco, Galapagos Island of San Cristobal Azolla megaspore and massulae Postglacial Galapagos Islands SEM 1.jpg
Scanning electron micrograph of a megaspore of the genus Azolla with adhering massulae from postal sediments of Laguna El Junco, Galápagos Island of San Cristóbal
Transmission electron micrograph of a megaspore of the genus Azolla from postglacial sediments of Laguna El Junco, Galapagos Island of San Cristobal Azolla megaspore Postglacial Galapagos Islands TEM longitudinal section 1.jpg
Transmission electron micrograph of a megaspore of the genus Azolla from postglacial sediments of Laguna El Junco, Galápagos Island of San Cristobal

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. [11]

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. [25] The barbed glochidia on the male spore clusters cause them to cling to the female megaspores, thus facilitating fertilization.

Applications

Food and animal feed

In addition to its traditional cultivation as a bio-fertilizer for wetland paddies, Azolla is finding increasing use for sustainable production of livestock feed. [26] 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. [27]

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. [28] Azolla may contain this substance that is a possible cause of neurodegenerative diseases, including causing ALS, Alzheimer's, and Parkinson's. [29] [30] [31] 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. [32] Previous studies attributed neurotoxin production to Anabaena flos-aquae species, which is also a type of nitrogen-fixing cyanobacteria. [33] 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”. [34] Further research may be needed to ascertain whether A. azollae is a healthy foodstuff for humans.

Companion plant

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. [35]

Larvicide

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". [18] 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. [36]

Climate change

Azolla has been proposed as a carbon sequestration modality. The proposal draws upon the hypothesized Azolla event that asserts that Azolla once covered the Arctic and then sank, permanently sequestering teratons of carbon that would otherwise have contributed to the planet's greenhouse effect and ending a warming event that reached 12–15 °C (22–27 °F) degrees warmer than twenty-first century averages. [37]

They contribute significantly to decreasing the atmospheric CO2 levels. [3]

Invasive species

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 30 centimetres (12 in) thick and cover 100% of a water surface, preventing local insects and amphibians from reaching the surface. [38]

Importance in paleoclimatology

A study of Arctic paleoclimatology reported that Azolla may have had a significant role in reversing an increase in greenhouse effect that occurred 55 million years ago that had caused the region around the north pole to turn into a hot, tropical environment. This research was conducted by the Institute of Environmental Biology at Utrecht University. It indicates that massive patches of Azolla growing on the (then) freshwater surface of the Arctic Ocean consumed enough carbon dioxide from the atmosphere for the global greenhouse effect to decline, eventually causing the formation of ice sheets in Antarctica and the current "icehouse period". This theory has been termed the Azolla event. [39]

Bioremediation

Azolla can remove chromium, nickel, copper, zinc, and lead from effluent. It can also remove lead from solutions containing 1–1000 ppm. [40]

Related Research Articles

<span class="mw-page-title-main">Spore</span> Unit of reproduction adapted for dispersal and survival in unfavorable conditions

In biology, a spore is a unit of sexual or asexual reproduction that may be adapted for dispersal and for survival, often for extended periods of time, in unfavourable conditions. Spores form part of the life cycles of many plants, algae, fungi and protozoa. They were thought to have appeared as early as the mid-late Ordovician period as an adaptation of early land plants.

A sporangium ; pl.: sporangia) is an enclosure in which spores are formed. It can be composed of a single cell or can be multicellular. Virtually all plants, fungi, and many other groups form sporangia at some point in their life cycle. Sporangia can produce spores by mitosis, but in land plants and many fungi, sporangia produce genetically distinct haploid spores by meiosis.

<span class="mw-page-title-main">Fern</span> Class of vascular plants

The ferns are a group of vascular plants that reproduce via spores and have neither seeds nor flowers. They differ from mosses by being vascular, i.e., having specialized tissues that conduct water and nutrients, and in having life cycles in which the branched sporophyte is the dominant phase.

<span class="mw-page-title-main">Aquatic plant</span> Plant that has adapted to living in an aquatic environment

Aquatic plants also referred to as hydrophytes are vascular plants and non-vascular plants that have adapted to live in aquatic environments. In lakes, rivers and wetlands, aquatic vegetations provide cover for aquatic animals such as fish, amphibians and aquatic insects, create substrate for benthic invertebrates, produce oxygen via photosynthesis, and serve as food for some herbivorous wildlife. Familiar examples of aquatic plants include waterlily, lotus, duckweeds, mosquito fern, floating heart, water milfoils, mare's tail, water lettuce, water hyacinth, and algae.

<span class="mw-page-title-main">Marsileaceae</span> Family of ferns

Marsileaceae is a small family of heterosporous aquatic and semi-aquatic ferns, though at first sight they do not physically resemble other ferns. The group is commonly known as the "pepperwort family" or as the "water-clover family" because the leaves of the genus Marsilea superficially resemble the leaves of a four-leaf clover. In all, the family contains three genera and 50 to 80 species with most of those belonging to Marsilea.

<i>Salvinia</i> Genus of aquatic plants

Salvinia or watermosses is a genus of free-floating aquatic ferns in the family Salviniaceae. The genus is named in honor of 17th-century Italian naturalist Anton Maria Salvini, and the generic name was first published in 1754 by French botanist Jean-François Séguier in Plantae Veronenses, a description of the plants found around Verona. Twelve species are recognized, at least three of which are believed to be hybrids in part because their sporangia are found to be empty.

<span class="mw-page-title-main">Heterocyst</span>

Heterocysts or heterocytes are specialized nitrogen-fixing cells formed during nitrogen starvation by some filamentous cyanobacteria, such as Nostoc, Cylindrospermum, and Anabaena. They fix nitrogen from dinitrogen (N2) in the air using the enzyme nitrogenase, in order to provide the cells in the filament with nitrogen for biosynthesis.

<i>Anabaena</i> Genus of bacteria

Anabaena is a genus of filamentous cyanobacteria that exist as plankton. They are known for nitrogen-fixing abilities, and they form symbiotic relationships with certain plants, such as the mosquito fern. They are one of four genera of cyanobacteria that produce neurotoxins, which are harmful to local wildlife, as well as farm animals and pets. Production of these neurotoxins is assumed to be an input into its symbiotic relationships, protecting the plant from grazing pressure.

<span class="mw-page-title-main">Microsporangium</span> Sporangia that produce spores that give rise to male gametophytes

A microsporangium is a sporangium that produces microspores that give rise to male gametophytes when they germinate. Microsporangia occur in all vascular plants that have heterosporic life cycles, such as seed plants, spike mosses and the aquatic fern genus Azolla. In gymnosperms and angiosperm anthers, the microsporangia produce microsporocytes, the microspore mother cells, which then produce four microspores through the process of meiosis. Microsporocytes are produced in the microsporangia of gymnosperm cones and the anthers of angiosperms. They are diploid microspore mother-cells, which then produce four haploid microspores by meiosis. These become pollen grains, within which the microspores divide twice by mitosis to produce a very simple gametophyte.

<span class="mw-page-title-main">Microspore</span> Small land plant spores that develop into male gametophytes

Microspores are land plant spores that develop into male gametophytes, whereas megaspores develop into female gametophytes. The male gametophyte gives rise to sperm cells, which are used for fertilization of an egg cell to form a zygote. Megaspores are structures that are part of the alternation of generations in many seedless vascular cryptogams, all gymnosperms and all angiosperms. Plants with heterosporous life cycles using microspores and megaspores arose independently in several plant groups during the Devonian period. Microspores are haploid, and are produced from diploid microsporocytes by meiosis.

<i>Azolla filiculoides</i> Species of plant

Azolla filiculoides is a species of aquatic fern. It is native to warm temperate and tropical regions of the Americas, and has been introduced to Europe, North and sub-Saharan Africa, China, Japan, New Zealand, Australia, the Caribbean and Hawaii.

<i>Azolla cristata</i> Species of aquatic plant

Azolla cristata , the Carolina mosquitofern, Carolina azolla or water velvet, is a species of Azolla native to the Americas, in eastern North America from southern Ontario southward, and from the east coast west to Wisconsin and Texas, and in the Caribbean, and in Central and South America from southeastern Mexico (Chiapas) south to northern Argentina and Uruguay.

<span class="mw-page-title-main">Azolla event</span> Hypothetical geoclimatic event

The Azolla event is a paleoclimatology scenario hypothesized to have occurred in the middle Eocene epoch, around 49 million years ago, when blooms of the carbon-fixing freshwater fern Azolla are thought to have happened in the Arctic Ocean. As the fern died and sank to the stagnant sea floor, they were incorporated into the sediment over a period of about 800,000 years; the resulting draw-down of carbon dioxide has been speculated to have helped reverse the planet from the "greenhouse Earth" state of the Paleocene-Eocene Thermal Maximum, when the planet was hot enough for turtles and palm trees to prosper at the poles, to the current icehouse Earth known as the Late Cenozoic Ice Age.

<i>Azolla primaeva</i> Extinct species of aquatic plant

Azolla primaeva is an extinct species of "water fern" in the family Salviniaceae known from Eocene fossils from the Ypresian stage, found in southern British Columbia.

<i>Azolla pinnata</i> Species of aquatic plant

Azolla pinnata is a species of fern known by several common names, including mosquitofern, feathered mosquitofern and water velvet. It is native to much of Africa, Asia and parts of Australia. It is an aquatic plant, it is found floating upon the surface of the water. It grows in quiet and slow-moving water bodies because swift currents and waves break up the plant. At maximum growth rate, it can double its biomass in 1.9 days, with most strains attaining such growth within a week under optimal conditions.

<i>Samea multiplicalis</i> Species of moth

Samea multiplicalis, the salvinia stem-borer moth, is an aquatic moth commonly found in freshwater habitats from the southern United States to Argentina, as well as in Australia where it was introduced in 1981. Salvinia stem-borer moths lay their eggs on water plants like Azolla caroliniana, Pistia stratiotes, and Salvinia rotundifolia. Larval feeding on host plants causes plant death, which makes S. multiplicalis a good candidate for biological control of weedy water plants like Salvinia molesta, an invasive water fern in Australia. However, high rates of parasitism in the moth compromise its ability to effectively control water weeds. S. multiplicalis larvae are a pale yellow to green color, and adults develop tan coloration with darker patterning. The lifespan, from egg to the end of adulthood is typically three to four weeks. The species was first described by Achille Guenée in 1854.

<i>Salvinia minima</i> Species of aquatic plant

Salvinia minima is a species of aquatic, floating fern that grows on the surface of still waterways. It is usually referred to as common salvinia or water spangles. Salvinia minima is native to South America, Mesoamerica, and the West Indies and was introduced to the United States in the 1920s–1930s. It is classified as an invasive species internationally and can be detrimental to native ecosystems. This species is similar to but should not be confused with giant salvinia, Salvinia molesta.

<i>Azolla mexicana</i> Species of aquatic plant

Azolla mexicana, the Mexican mosquito fern, is an aquatic fern native to Mexico, British Columbia and the western United States.

<i>Azolla nilotica</i> Species of aquatic plant

Azolla nilotica is a medium-sized floating fern, that naturally occurs in the Nile and in eastern and central Africa. It is assigned to the family Salviniaceae.

References

  1. ↑ Currently Trichormus azollae (Strasburger 1884) Komárek and Anagnostidis 1989. Synonyms: Nostoc azollaeStrasburger 1883, Anabaena azollaeStrasburger 1884, Desikacharya azollae(Strasburger 1884) Saraf et al. 2019.
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    Type Specimens HT: Azolla filiculoides
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  38. ↑ "Invasive non-native species (UK) – Water fern". Inside Ecology. November 1, 2017.
  39. ↑ "Can A Tiny Fern Help Fight Climate Change and Cut Fertilizer Use?". Yale E360. July 11, 2018. Retrieved November 25, 2021.
  40. ↑ Robert L. Irvine; Subhas K. Sikdar (January 8, 1998). Bioremediation Technologies: Principles and Practice. CRC Press. p. 102. ISBN   9781566765619.
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