B I O D I V E R S I T YVol. 12, No. 2, June 2011, 119–128

BLOSSOMING TREASURES OF BIODIVERSITY

35. Mosquito Ferns (Azolla species) – tiny ‘super plants’

Ernest Small* and Stephen J. Darbyshire

Biodiversity, National Program on Environmental Health,Agriculture and Agri-Food Canada, Ontario, Ottawa,

Canada K1A 0C6

Introduction

Biodiversity is threatened by humankind’s continuingusurpation of our planet’s physical space and resources,and the associated damage to the landscape andatmosphere. Food production is widely acknowledgedto be the most important human activity that needs tobe addressed in order to mitigate the current biodiver-sity and environmental crises. In this contribution wefeature obscure plants called Mosquito Ferns, whoseminute size belies their incredible potential. Nicknamed‘super plants’, these can not only produce food morerapidly than virtually any other life form, but do so inbiodiversity-friendly ways that minimise use of spaceand energy resources. Mosquito Ferns are poised tobecome leading players in the search for sustainablerelationships with the natural world.

The plants

Azolla, with about five extant species, is the only genusin the Azollaceae, a small family of ferns (which issometimes combined with the genus Salvinia in thefamily Salviniaceae). The delimitation of species ofAzolla and determination of their correct names israther unsettled. The species reproduce primarily bybudding off new plants. Sexual reproductive structures(described below) are usually absent, and withoutthem it is very difficult to identify the species withcertainty. Mosquito Ferns are sometimes mistaken forDuckweeds (Lemnaceae), a family of about five generaand 40 species of flowering plants, which are also tinyaquatic plants of worldwide distribution. Some speciesof Duckweeds are floating, whereas others are sub-mersed in the water. Duckweeds are the smallest of allflowering plants, but they rarely produce flowers andseeds and, like Mosquito Ferns, reproduce mostly bybudding off new plants.

Mosquito Ferns (often ‘‘Mosquito-ferns’’) are alsofrequently called Azolla, Duckweed Fern, Fairy Moss(the plants have a moss-like appearance), MosquitoPlant and Water Fern. Species of Salvinia are morefrequently called Water Ferns, so this name should beavoided. The name ‘Mosquito Fern’ is said to havearisen because thick mats of floating plants have areputation for preventing mosquitoes from laying eggs.The curious genus name Azolla is based on the Greekazo, to dry! ollyo, to kill, an allusion to death fromdrought, which occurs should the plants lose theirsupply of water.

Azolla species are diminutive, delicate, free-floating,annual plants. The extremely small leaves (technically‘fronds’ in ferns), no larger than 2mm or 0.08 inchacross, are alternately attached to the branching stems,often overlapping in two ranks. Mosquito Ferns aremuch reduced in form, and do not exhibit the charac-teristic highly dissected (‘ferny’) foliage of most ferns.The leaves have an upper green (i.e. photosynthetic)lobe, which bears hydrophobic hairs, and a smaller,usually colourless lobe, which is buoyant and oftensubmersed. Thread-like, unbranched roots are pro-duced from the axils of branches. Under good condi-tions the plants can grow over each other in layers anddevelop mats up to 5 cm (2 inches) thick. Most speciesof Azolla produce reddish pigments when stressed, forexample by temperature extremes or feeding damage byherbivores, and this may result in a pinkish or reddishcarpet of plants covering expanses of water. Azollafiliculoides has been called Red Water Fern because ofthe tendency to become reddish.

Perhaps the most remarkable feature of Azollaspecies is their symbiosis with a bacterial partner.The upper leaf lobes house the bacteria in a pouch ontheir lower side. This tightly integrated relationship isunique in the plant world.

Ferns reproduce by spores, not seeds. Most fernspecies have just one kind of spore, but Azolla has two

*Corresponding author. Email: ernie.small@agr.gc.ca

ISSN 1488–8386 print/ISSN 2160–0651 online

Her Majesty the Queen in Right of Canada, as represented by the Minister of Agriculture and Agri-Food Canada (2011).DOI: 10.1080/14888386.2011.585928http://www.informaworld.com

Dow

nloa

ded

by [A

gric

ultu

re &

Agr

i-Foo

d Ca

nada

], [E

rnes

t Sm

all]

at 0

6:04

17

Nov

embe

r 201

1

kinds, in reproductive structures termed sporocarps,which are developed at the junctions of the lower leaflobes with the branches. Male sporocarps are minute(about 2mm or 0.08 inch in diameter) and produce malespores, which adhere to each other in clumps; femalesporocarps are smaller than the male sporocarps, eachproducing just one viable female spore, which is muchlarger than the individual male spores. Arrowhead-likebarbs on the clumps of male spores seem to assist inadhering to the female spores. Each male sporeproduces eight swimming sperms, some of whichsucceed in fertilising the females.

In China and Vietnam, particular strains ofA. pinnata are cultivated in rice culture systems, asdiscussed below. Whether such strains have been‘domesticated’ (changed genetically from wild ances-tors), or simply represent selections of forms that existin the wild, is undetermined. Some recent success hasbeen achieved in selecting and recombining moreproductive forms of fern-bacterium partnerships.

Figure 1. Mosquito Fern (Azolla caroliniana) plants. Photosby S. Darbyshire.

Figure 2. Floating mats of Mosquito Ferns. Left: Azolla caroliniana; photo by S. Darbyshire. Right: Azolla pinnata var.imbricata; credit: Show-ryu (public domain photo).

Figure 3. Azolla microphylla. Source: Cody, W.J. andBritton, D.M. 1989. Ferns and fern allies of Canada.Agriculture Canada, Ottawa.

120 E. SMALL AND S.J. DARBYSHIRE

Dow

nloa

ded

by [A

gric

ultu

re &

Agr

i-Foo

d Ca

nada

], [E

rnes

t Sm

all]

at 0

6:04

17

Nov

embe

r 201

1

The North American species of Azolla have not beenemployed to any appreciable extent in agriculture, butit is possible that strains that grow well in aquaria havebeen unconsciously selected.

Geography and ecology

Mosquito Ferns are freshwater aquatic plants oftemperate and tropical regions. Generally, the speciesoccur in stagnant or slow-moving waters, such asfound in ponds, lakes, marshes, swamps and somestreams. Occasionally the plants are stranded on wetmud, but normally they float on the surface of water,the roots hanging down. The plants have limitedtolerance of freezing temperatures and saline water(although some species can tolerate about 1% saltconcentration and A. filiculoides can grow in 2.5%saline solution).

Three species of Mosquito Ferns are native to theAmericas: A. caroliniana, A. microphylla (includingA. mexicana) and A. filiculoides. Azolla caroliniana isnative to southeastern Canada, the eastern half of theUS, the Caribbean, Central America and SouthAmerica. It has also become naturalised elsewhere.This is the most cold-tolerant of Azolla species, capableof surviving hard frosts and prolonged coverage by ice.It is also the most adapted to survival on mud. Azollafiliculoides is native to western North America, gener-ally in areas near the Pacific Ocean. It is also native toSouth America, and has been become naturalised inmuch of the remainder of the world. This species is alsocold-tolerant, and can survive under thin ice. Azollamicophylla is native to southwestern Canada, the

western US, Central America, South America, and theWest Indies. Azolla pinnata (including A. rubra), calledWater Velvet and Ferny Azolla, is native to Africa,Australia, and Asia. Azolla nilotica is native to Africa.

The weed problem

Azolla species are commonly grown as ornamentals inaquaria, where they provide hiding places for smallfish. Plants discarded from aquaria account for theoccasional appearance of Mosquito Ferns outside oftheir native distribution areas. In parts of the

Figure 4. World distribution of Azolla species.

Figure 5. Anabaena azollae, the nitrogen-fixing cyanobacte-rium which forms a symbiotic relationship with MosquitoFerns. The large cells within the filaments are ‘heterocysts’(arrows point to three of these), special cells that synthesiseorganic nitrogen compounds from the nitrogen in the air.The smaller cells are photosynthetic. Photo by S. Darbyshire.

B I O D I V E R S I T Y 121

Dow

nloa

ded

by [A

gric

ultu

re &

Agr

i-Foo

d Ca

nada

], [E

rnes

t Sm

all]

at 0

6:04

17

Nov

embe

r 201

1

United States, the introduced A. pinnata has beendeclared a noxious weed, and shops that marketaquatic plants are subject to penalties for distributingit, even inadvertently. In some areas of the world,including Australia and New Zealand, Mosquito Fernsare significant weeds.

Nitrogen ecology

Mosquito Ferns are associated with a bacterium in asymbiotic relationship. The bacterium developsunbranched filaments which are divided into cell-likesegments, with occasional segments that are larger andless pigmented, where nitrogen fixation occurs asdescribed below. The bacterium is widely identified asAnabaena azollae, a member of an important groupof photosynthetic bacteria called cyanobacteria (thesebacteria are also known as blue-green algae because ofthe colour of the pigments responsible for photosyn-thesis). Controversy regarding the identification of thesymbiotic associate of Mosquito Ferns as Anabaena,and whether there are other bacterial associates, isdiscussed below. The fern furnishes protection andprobably some nutrients to the bacterium, while thelatter provides nitrogen to the fern, as noted below. Thebacterium occurs in cavities in the leaves, in the growingpoints of the stems, and on other parts of the plant.When the plant reproduces by spores, the bacteriumbecomes associated with a specific area (the ‘indusialcap’) on top of the megaspore (the female reproductivestructure). Symbiotic associations between plants andnitrogen-fixing bacteria are common, but the Azolla–Anabaena association is unique in that the bacteriumcannot reproduce in nature outside of its host, the fern.No other plant–cyanobacterium symbiosis is knownwith a comparably precise mechanism that guaranteestransfer of the bacterium from one plant to its offspring(in other symbioses, plants developing from seeds mustacquire their bacterial partner from free-living bacteriain the environment).

The bacterium fixes atmospheric nitrogen; that is, itconverts inert gaseous nitrogen into a chemicallycombined form that the plants can metabolise. Sincenitrogen is a critical nutrient for living things, and isalmost always insufficiently available in soil (or water)for optimum plant growth, this provides MosquitoFerns with a tremendous advantage. There are as manyas 10,000 species of ferns, but only Azolla species areknown to be symbiotically associated with nitrogen-fixing organisms. (Nitrogen-fixing microbial symbiontsare best known in association with species in the Peafamily, but a variety of unrelated plants and even someanimals have such relationships.) As a result, MosquitoFerns can grow very rapidly, under ideal conditions

doubling their biomass every two to five days.Insufficient phosphorus in water is usually the chieflimiting factor for Mosquito Fern growth, and whenchemical runoff (such as from fertilisers and sewage)enriches water with phosphorus, the result may bespectacular carpeting of bodies of water with MosquitoFern plants (algal blooms similarly result from such‘eutrophication’ of water). Phosphorus-based deter-gents are well known as a cause of eutrophication.

Most literature identifies the symbiotic nitrogen-fixing associate of Azolla as Anabaena azollae.However, since the 1990s this has been challenged.It has been claimed that the species belongs to Nostoc,another genus of blue-green algae. Others claim arethat the cyanobacterium species present is neitherAnabaena azollae nor Nostoc. It has been demonstratedthat additional cyanobacteria are present in smallquantities in some Azolla species, and some kinds ofnon-photosynthetic bacteria are also present; the roles,if any, of these other bacteria is uncertain.

Although Azolla species and Anabaena azollae arepermanently associated with each other (the bacteriumhas not been found outside of the plant and the plant isalmost always accompanied by the bacterium),Mosquito Fern roots have retained the capacity toextract nitrogen from their environment. Interestingly,when the bacterium has been experimentally killed off(using antibiotics), the plant compensates for theloss of bacterium-supplied nitrogen by developingextra roots.

‘Because of the growing concern about conservationof the environment and the need for deployingrenewable, sustainable resources, the application ofAzolla as a biofertiliser on agricultural crops, in orderto provide a natural source of the crucial nutrient, canbe very benefical to the future of our planet.’

—G.M. Wagner (1997)

Organic vs. chemical fertilisation

Nitrogen is the element that is most often the limitingfactor in plant growth, and the addition of nitrogen isusually the most efficient way of increasing cropproduction. Although the atmosphere is almost 80%nitrogen, plants (and animals) cannot use it in thegaseous form, N2. Bacteria, particularly nitrogen-fixingbacteria (mostly free-living, some symbiotically associ-ated with certain plant species), are able to convertgaseous, inert nitrogen to ammonium ions (NH!4 ) ornitrate ions (NO"3 ), which plants can then utilise.

In the early 20th century, chemists discovered howto generate nitrogenous fertilisers from atmosphericnitrogen, and such synthetic fertilisers now dominateagriculture. Unfortunately there are associated

122 E. SMALL AND S.J. DARBYSHIRE

Dow

nloa

ded

by [A

gric

ultu

re &

Agr

i-Foo

d Ca

nada

], [E

rnes

t Sm

all]

at 0

6:04

17

Nov

embe

r 201

1

negative effects: (1) the production of these fertilisersrequires considerable expenditure of energy, includingthe need for transportation; (2) the production ofchemical fertilisers is alarmingly consumptive of fossilfuels: for every unit of nitrogen fertiliser produced, twounits of petroleum are required; (3) plants cannotabsorb all applied fertiliser, so much of it leaches intothe air, soil, and water, significantly reducing microbialactivity in soil, and exposing numerous plants andanimals to atmospheric and water-born toxins.Nitrogen fertilisers may account for about one-thirdof greenhouse gases. In particular, a significant pro-portion of the fertiliser volatilises as nitrous oxide(N2O), contributing to atmospheric pollution and theglobal greenhouse gas problem. Nitrous oxide absorbsinfrared radiation in the atmosphere, causing atmo-spheric warming, and it can also combine with oxygenin the stratosphere to form nitrogen monoxide, whichreacts with ozone and decreases the ozone layer.Still another undesirable gas that results from theapplication of chemical fertilisers is gaseous ammonia(NH3), which leads to eutrophication and acidificationof natural ecosystems. It has been shown that theproduction of ammonia is substantially decreasedwhen Mosquito Ferns are added to chemically-fertilised rice paddies.

The key to reducing the undesirable effects ofsynthetic fertilisers on ecosystems is their replace-ment with ‘biofertilisers’. The use of natural, organic

material to encourage growth of plants amountsto mimicking nature, and has many advantages.Properly applied, natural fertilisers are non-polluting,supply a much wider range of nutrients to plants thando synthetic fertilisers, and improve soil structure andthe welfare of soil biota. Moreover, organic materialdecays slowly, providing long-term benefits. Organicfertilisers require more elaborate storage and applica-tion, and increased labour compared to chemicalfertilisers, explaining why synthetic fertilisers arewidespread in industrialised nations, while naturalfertilisers are popular in developing countries.However, the growing financial costs and increasingecological and health damage associated with indus-trial fertilisers suggest that natural fertilisers willbecome increasingly important.

The use of Azolla as an organic fertiliser in place ofsynthetic fertilisers has great potential to reduce theworld’s reliance on fossil fuels. While Mosquito Fernshave many uses, they are most important as bioferti-lisers or ‘green manure’, especially in Southeast Asiaand in other rice-producing regions of the world.Shortly after Rice is planted, the paddies are ofteninoculated with Azolla, which multiples rapidly tocover the water, serving to suppress weeds. Moreimportantly, as the Mosquito Ferns die and disinte-grate, the nitrogen that their bacterial partners havefixed is released to the Rice plants, contributing greatlyto growth of the crops. Rice and Wheat are the world’s

Figure 6. Common species used in organic shallow-water food-producing systems in Asia. Rice, the chief crop, benefits from thepresence of the other species, as discussed in the text. The Mosquito Ferns provide organic fertilisation for the Rice plants, andalso provide food for plant-eating ducks and fish, and for livestock. All of these species ultimately are eaten by people. Preparedby B. Brookes.

B I O D I V E R S I T Y 123

Dow

nloa

ded

by [A

gric

ultu

re &

Agr

i-Foo

d Ca

nada

], [E

rnes

t Sm

all]

at 0

6:04

17

Nov

embe

r 201

1

most important food crops, but Rice is a staple foodfor more people than any other crop. In China alone,over 1.2 million ha (3 million acres) of Rice are grownwith Azolla, which is thought to more than doubleproductivity. Harvested Azolla is also used to someextent as a mulch and as a fertiliser for terrestrially-grown crops. Various systems and cultural practiceshave been devised to maximise the benefits ofAzolla use given situations, goals and constraints ofthe farm system.

Integrated farming systems

‘Polyculture’ has been described as a ‘species-diversi-fied cropping system’; it is the simultaneous culture ofeconomically useful plants and possibly also animals.‘Aquaponics’ is a special kind of polyculture: thecombined cultivation of plants and animals in water toproduce food (and sometimes other useful products).In Asia, Azolla is commonly grown in rice fields notjust to increase rice yield but also simultaneously tofeed aquatic animal species such as fish (notablyTilapia, Loach, and Grass Carp), shrimp, ducks, andgeese, which simply consume the Mosquito Ferns.In such systems, Azolla serves as a nitrogen source forthe plants and a food source for the animals. Excretafrom the animals reinforce the fertilisation of theplants. The animals also tend to feed upon and destroyweeds and insect pests that harm the planted crop.As a small, floating plant, Azolla grows below theleaves of aquatic plants such as Rice, and so does notcompete for light and space with the crop. As the ricecrop approaches maturity, its shade kills the Azolla,which decomposes very rapidly, providing nitrogenand other elements just as the Rice increasesits demand for nutrients for grain maturation.With such complex systems, considerable knowledgeis necessary in order to ensure that the elements worktogether; in the case of the Rice–Azolla–livestocksystem, as much as 2000 years of practical experiencein Asia have provided the required knowledge.

Eco-farming

‘Eco-farming’ and ‘agro-ecology’ are phrases that haverecently been applied to the use of sustainable agricul-tural techniques that are relatively friendly to theenvironment and biodiversity. In contrast to ‘factoryfarming’ that is based on monocultured crops dousedwith chemical fertilisers and pesticides, resulting indegradation of soils and fuelling climate change, eco-farming and agro-ecology tend to be small-scale, basedon a diverse mix of crops, especially those thatcontribute nitrogen to the soil. The integrated farming

system described in the preceding is an excellentexample of this philosophy. A recent United Nationsreport very strongly recommends this approach as ameans of simultaneously addressing the growing threatof hunger in much of the Developing World as well asthe growing threats to biodiversity and the environment(see: http://www.srfood.org/images/stories/pdf/press_releases/20110308_agroecology-report-pr_en.pdf ).

Livestock feed

Mosquito Ferns are also agriculturally important asfodder and forage for livestock, including cattle, pigs,goats, ducks, geese and chickens. Harvested Azolla issimply added as a nutritional supplement to the regularfeed of mammals and poultry. In some areas of Africa,natural, wild growths of Mosquito Ferns have beenharvested from lakes and ponds. In Asia, however,techniques for growing Mosquito Ferns in smallartificial ponds as well as natural water bodies arevery well developed.

Human food potential

Azolla is thought to be suitable for human consump-tion, although to date only experimental preparationof food products has been attempted. Nitrogen isessential in proteins, and plant species that are asso-ciated with nitrogen-fixing bacteria are usually rich inprotein. Indeed, Mosquito Ferns are very rich inprotein, as much as a quarter of their dry weight. Theamino acid profile (a measure of protein quality) isgood, although there are minor deficiencies of methi-onine, cysteine, and lysine.

Erik Sjodin of Sweden has recently conductedexperimental preparation of foods based on Mosquito

Figure 7. A pony enjoying a meal of Mosquito Fern. Photocourtesy of E. Sjodin.

124 E. SMALL AND S.J. DARBYSHIRE

Dow

nloa

ded

by [A

gric

ultu

re &

Agr

i-Foo

d Ca

nada

], [E

rnes

t Sm

all]

at 0

6:04

17

Nov

embe

r 201

1

Ferns (http://www.eriksjodin.net). He has kindlyallowed us to reproduce his recipe for ‘Azollaburgers’:

Ingredients:100 g of fresh Azolla (or 50 g of fried Azolla)Breadcrumbs (a required binder)Salt, pepper, fresh herbs

(1) Fry fresh Azolla in a pan for 1–2 minutes.(2) Chop the fried Azolla, and mix it with spices

and herbs.(3) Mix in breadcrumbs until the mixture can be

formed into burgers.(4) Fry the burgers in vegetable oil.

Mosquito control

Another use of Mosquito Ferns is as a destroyer ofmosquito larvae. Mosquito larvae are aquatic organ-isms, but must come to the water surface to obtainoxygen. A thick carpet of Azolla reduces the ability ofthe larvae to reach the surface to breathe. It has alsobeen shown that a thick floating carpet of the plantsreduces deposition of eggs by mosquitoes. Mosquito-borne diseases, especially malaria, may be reduced byincreasing the cultivation ofAzolla. AlthoughMosquito

Ferns have been demonstrated to be capable of reducingMosquito populations to some extent, doubt has beenexpressed that the overall effect is significant.

Water purification

Azolla has been found to have potential value as a‘nutrient mop’ for treating waste water. MosquitoFerns are especially efficient in removing phosphatesfrom water, a chief contributor to algal blooms. Unlikealmost all other aquatic plants, Mosquito Ferns arenot limited by lack of nitrogen, and in nitrogen-deficient waters they are especially useful for removingunwanted chemicals. The most promising remedialapplication of Azolla is the removal from contaminatedwater of heavy metals, such as chromium, cadmium,and nickel. Because of the ease of harvesting, it may bepossible to efficiently recover the accumulated metalsonce they have been absorbed by the plants.

Experimental fuels

In the 1970s, it was discovered that Anabaena azollauses light energy to release hydrogen from water.

Figure 8. Photos showing experimental culinary preparations of Mosquito Fern. Photos courtesy of E. Sjodin.

B I O D I V E R S I T Y 125

Dow

nloa

ded

by [A

gric

ultu

re &

Agr

i-Foo

d Ca

nada

], [E

rnes

t Sm

all]

at 0

6:04

17

Nov

embe

r 201

1

Under natural conditions, this hydrogen is immedi-ately combined with the nitrogen that is fixed by thebacterium to produce ammonia, which is subsequentlyprovided to the host fern as its nitrogen source. It hasbeen shown that when Azolla and its symbiotic partnerare grown under certain conditions (for example, in anatmosphere that excludes nitrogen), the cyanobacte-rium produces stable hydrogen gas from water.Hydrogen gas can be used as a non-polluting, high-energy fuel. Indeed, hydrogen can produce moreenergy than any other non-nuclear fuel, and ifproduced on a large scale, could be extremely impor-tant in addressing the problem of dwindling petroleumreserves. This phenomenon has not yet resulted in apractical application, but the possibility of this isintriguing.

Another interesting experimental finding is thatAzolla can be fermented anaerobically (in theabsence of oxygen) to produce methane gas, whichmight also be used as fuel. Mosquito Ferns maybe more productive than most current terrestrialbiofuel crops.

Prospects

Mosquito Ferns are extremely important as effi-ciently generated feed for production of meat,poultry, fish, and shrimp, and they have potentialfor directly generating human food, and also pro-ducing biofuels. Their value as biofertilisers thatsubstitute for synthetic fertilisers and thereby reducethe use of fossil fuels is immense. As the humanpopulation continues to outpace increases in foodproduction, Azolla is likely to become increasinglysignificant.

Believe it or not

. Particular pigments in photosynthetic cellscapture a small range of photosyntheticallyactive light. One of the secrets of the very highproductivity of Azolla is the fact that the light-capturing pigments in the plants (chlorophylla and b, and carotenoids) complement thelight-capturing pigments in the bacterial part-ner (chlorophyll a and phycoblins) to capturemost of the visible light in the 500 to 700 nmspectrum. This allows the partners to capturea wider range of the sunlight’s wavelengthsthan either could alone.

. Since Mosquito Ferns are aquatic plants, it isnot surprising that the water content of theplants is high: 85–95%.

. According to a Vietnamese legend, 300 yearsago a Vietnamese woman named Ba Hengdiscovered that the presence of MosquitoFerns in rice paddies increased production.In her honour, an annual festival in the fall isstill celebrated.

. ‘Water fern cake’ or beo cake (banh beo) is aVietnamese speciality, which is not made withMosquito Ferns, despite the name. It is,however, named for its resemblance toMosquito Ferns floating on water. Waterfern cake is a thin, steamed rice cake, the topstuffed with minced shrimp, scallions, greenbean paste, and fried shallots.

. The ‘Azolla Event’ is a spectacular climatechange thought to have been triggered byAzolla in ancient times, when several dozennow extinct species of Mosquito Fernsoccurred. Following the elimination of thedinosaurs about 65 million years ago, theclimate of Earth became very different fromthat of today. Fifty-five million years ago,Earth had a hot (up to 12#C or 22#F warmerthan today), tropical climate, with palm treesgrowing at both poles. This is believed to haveresulted from increased carbon dioxide in theatmosphere, caused in part by extensive vol-canism, and consequent heating by the green-house effect. It is hypothesised that extensive,dense patches of Azolla developed in freshwa-ter lakes in the Arctic area, and perhaps alsoin the Arctic Ocean (which at the time wasalmost completely enclosed by land, andconsequently was less saline than todaybecause of the inflow of water from rivers).Because of the heat and the very highlevels of carbon dioxide, incredible growth of

Figure 9. A young girl being introduced to Mosquito Fern.Photo courtesy of E. Sjodin.

126 E. SMALL AND S.J. DARBYSHIRE

Dow

nloa

ded

by [A

gric

ultu

re &

Agr

i-Foo

d Ca

nada

], [E

rnes

t Sm

all]

at 0

6:04

17

Nov

embe

r 201

1

Mosquito Ferns took place. It has beenestimated that as the plants died, layersof dead plants up to 8m (26 feet) accumu-lated on the ocean floor (cold temperaturesat the bottom of deep waters is thought tohave prevented decay of the MosquitoFerns). This removal (‘sequestration’) ofcarbon dioxide by the Mosquito Fernsreduced the greenhouse effect and so cooledthe planet. Carbon dioxide levels in theatmosphere are thought to have droppedfrom 3500 parts per million to about650 ppm, the world turned cold, ice capsformed at both poles, and sea level dropped.This cold phase has been maintained untiltoday, but now global warming is threateningto reverse the situation.

. In the flowering or seed plants, non-swimmingsperm are delivered to the egg by a tube thatdevelops from the pollen grain, penetratesthe stigma, and grows directly to the egg.By contrast, animals, including humans, havesperm which swim to reach and fertilise eggs.Swimming sperm are also present in themore primitive classes of plants: algae,mosses, cycads, Ginkgo, and ferns (includingMosquito Ferns).

. Azolla is one of the fastest-growing plants onEarth, capable of producing 9 tonnes ofprotein per hectare (4 tonnes per acre). It hasbeen suggested that growing plants like Azollafor human food could require only about 200square metres (239 square yards or about halfan acre) of land to feed an average human—less than one hundredth of the area nowrequired for the average American. Suchremarkable growth has made Azolla one ofthe principal plant species that is being con-sidered for food production during spacevoyages and for colonising the universe.

Acknowledgements

We thank Erik Sjodin for providing photos and information,and Brenda Brookes for preparing figures.

Key information sources

Bennicelli, R., Z. Stepniewska, A. Banach, K. Szajnocha, andJ. Ostrowski. 2004. The ability of Azolla caroliniana toremove heavy metals (Hg(II), Cr(III), Cr(VI)) frommunicipal waste water. Chemosphere 55: 141–6.

Darbyshire, S.J. 2002. Ephemeral occurrence of the mosquitofern, Azolla caroliniana, at Ottawa, Ontario. CanadianField-Naturalist 116: 441–5.

Ekman, M., P. Tollback, and B. Bergman. 2008.Proteomic analysis of the cyanobacterium of theAzolla symbiosis: identity, adaptation, and NifHmodification. Journal of Experimental Botany 59:1023–34.

Evrard, C., and C. Van Hove. 2004. Taxonomy of theAmerican Azolla species (Azollaceae): a criticalreview. Systematics and Geography of Plants 74:301–18.

Furuno, T. 2001. The power of duck: integrated rice and duckfarming. Sisters Creek, Tasmania, Australia: TegariPublications.

Kannaiyan, S., and K. Kumar. 2005. Azolla biofertilizer forsustainable rice production. Delhi: Daya PublishingHouse.

Khan, M.M. 1983. A primer on Azolla production andutilization in agriculture. Los Banos, Phillippines:University of the Philippines at Los Banos.

Lejeune, A., A. Cagauan, and C. Van Hove. 1999. Azollaresearch and development: recent trends and priorities.Symbiosis 27: 333–51.

Lumpkin, T.A. 1993. Azollaceae. In Flora ofNorth America, Vol. 2, ed. Flora of North AmericaEditorial Committee, 338–42. New York: OxfordUniversity Press.

Lumpkin, T.A., and D.L. Plucknett. 1980. Azolla: botany,physiology, and use as a green manure. Economic Botany34: 111–53.

Lumpkin, T.A., and D.L. Plucknett. 1982. Azolla as a greenmanure: use and management in crop production.Westview Tropical Agriculture Series, No. 5. Boulder,CO: Westview Press.

Metzgar, J.S., H. Schneider, and K.M. Pryer. 2007.Phylogeny and divergence time estimates for the ferngenus Azolla (Salviniaceae). International Journal ofPlant Science 168: 1045–53.

Moore, A.W. 1969. Azolla: biology and agronomic signifi-cance. The Botanical Review 35: 17–35.

Papaefthimiou, D., C. Van Hove, A. Lejeune, U. Rasmussen,and A. Wilmotte. 2008. Diversity and host specificity ofAzolla cyanobionts. Journal of Phycology 44: 60–70.

Peters, G.A., and J.C. Meeks. 1989. The Azolla-Anabaena symbiosis: basic biology. Annual Review ofPlant Physiology and Plant Molecular Biology 40:193–210.

Reid, J.D., G.M. Plunkett, and G.A. Peters. 2006.Phylogenetic relationships in the heterosporous ferngenus Azolla (Azollaceae) based on DNA sequencedata from three noncoding regions. InternationalJournal of Plant Science 167: 529–38.

Saunders, R.M.K., and K. Fowler. 1992. A morphologicaltaxonomic revision of Azolla Lam. section Rhizosperma(Mey.) Mett. (Azollaceae). Botanical Journal of theLinnean Society 109: 329–57.

Saunders, R.M.K., and K. Fowler. 1993. The supraspecfictaxonomy and evolution of the fern genus Azolla(Azollaceae). Plant Systematics and Evolution 184:175–93.

Speelman, E.N., M.M.L. van Kempen, J. Barke,H. Brinkhuis, G.J. Reichart, A.J.P. Smolders,

B I O D I V E R S I T Y 127

Dow

nloa

ded

by [A

gric

ultu

re &

Agr

i-Foo

d Ca

nada

], [E

rnes

t Sm

all]

at 0

6:04

17

Nov

embe

r 201

1

J.G.M. Roelofs, F. Sangiorgi, J.W. De Leeuw,A.F. Lotter, and J.S. Sinninghe Damste. 2009.The Eocene Arctic Azolla bloom: environmental condi-tions, productivity and carbon drawdown. Geobiology 7:155–70.

Van Cat, D., I. Watanabe, W.J. Zimmerman, T.A. Lumpkin,and T. De Waha Baillonville. 1989. Sexual hybridization

among Azolla species. Canadian Journal of Botany 67:3482–5.

Wagner, G.J. 1997. Azolla: a review of its biology andutilization. The Botanical Review 63: 1–26.

Zimmerman, W.J., T.A. Lumpkin, and I. Watanabe. 1989.Classification of Azolla spp., section Azolla. Euphytica43: 223–32.

128 E. SMALL AND S.J. DARBYSHIRE

Dow

nloa

ded

by [A

gric

ultu

re &

Agr

i-Foo

d Ca

nada

], [E

rnes

t Sm

all]

at 0

6:04

17

Nov

embe

r 201

1