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, duckweed fern, fairy moss, water fern) 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 duckweed or some mosses. 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 DM/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 , 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 this genus and of the family Azollaceae in Tasmania. It is a common native aquatic plant in Tasmania. It is common 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. [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] Further research may be needed to ascertain if A. azollae produces neurotoxins.

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 A.D 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. [34]

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. [35]

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. [36]

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. [37]

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. [38]

Bioremediation

Azolla can remove chromium, nickel, copper, zinc, and lead from effluent. It can also remove lead from solutions containing 1–1000 ppm. [39]

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.

<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.

<i>Isoetes</i> Genus of vascular plants in the family Isoetaceae

Isoetes, commonly known as the quillworts, is a genus of lycopod. It is the only living genus in the family Isoetaceae and order Isoetales. There are currently 192 recognized species, with a cosmopolitan distribution mostly in aquatic habitats but with the individual species often scarce to rare. Some botanists split the genus, separating two South American species into the genus Stylites, although molecular data place these species among other species of Isoetes, so that Stylites does not warrant taxonomic recognition. Species virtually identical to modern quillworts have existed since the Jurassic epoch, though the timing of the origin of modern Isoetes is subject to considerable uncertainty.

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

Aquatic plants are plants that have adapted to living in aquatic environments. They are also referred to as hydrophytes or macrophytes to distinguish them from algae and other microphytes. A macrophyte is a plant that grows in or near water and is either emergent, submergent, or floating. In lakes and rivers macrophytes provide cover for fish, substrate for aquatic invertebrates, produce oxygen, and act as food for some fish and wildlife.

<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 3 genera and 50 to 80 species with most of those belonging to Marsilea.

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

Salvinia, a genus in the family Salviniaceae, is a floating fern named in honor of Anton Maria Salvini, a 17th-century Italian scientist. Watermoss is a common name for Salvinia. The genus was published in 1754 by Jean-François Séguier, in his description of the plants found round Verona, Plantae Veronenses 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.

Diazotrophs are bacteria and archaea that fix atmospheric nitrogen(N2) in the atmosphere into bioavailable forms such as ammonia.

<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 (pl. microsporangia) 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.

<span class="mw-page-title-main">Megaspore</span> Large spore in heterosporous plants that germinates into a female gametophyte

Megaspores, also called macrospores, are a type of spore that is present in heterosporous plants. These plants have two spore types, megaspores and microspores. Generally speaking, the megaspore, or large spore, germinates into a female gametophyte, which produces egg cells. These are fertilized by sperm produced by the male gametophyte developing from the microspore. Heterosporous plants include seed plants, water ferns (Salviniales), spikemosses (Selaginellaceae) and quillworts (Isoetaceae).

<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.

β-Methylamino-<small>L</small>-alanine Chemical compound

β-Methylamino-L-alanine, or BMAA, is a non-proteinogenic amino acid produced by cyanobacteria. BMAA is a neurotoxin. Its potential role in various neurodegenerative disorders is the subject of scientific research.

<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>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

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    Type Specimens HT: Azolla filiculoides
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