Azolla

Datasheet

Description

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Common names

Azolla, mosquito fern, duckweed fern, fairy moss, water fern [English]; helecho mosquito, helecho de pato, helecho de agua [Spanish]; Algenfarne [German]; bèo hoa dâu [Vietnamese]; 满江红 [Chinese]; अजोला [Hindi]; アカウキクサ属 [Japanese]; അസോള [Malayalam]; آزیریان [Persian]; Азолла [Russian]; அசோலா [Tamil]; แหนแดง [Thai]

Species

Azolla caroliniana Willd. ; Azolla filiculoides Lam. ; Azolla mexicana C.Presl ; Azolla microphylla Kaulf. ; Azolla nilotica Decne. ex Mett. ; Azolla pinnata R. Br. [Azollaceae]

Taxonomic information

Azolla taxonomy is debated. The Azolla genus contains 5 or 7 species, and is placed either in the Salviniaceae or in the Azollaceae family.

Related feed(s)

Description

Azolla (Azolla sp.) is an aquatic fern consisting of a short, branched, floating stem, bearing roots which hang down in the water. The leaves are alternately arranged, each consisting of a thick aerial dorsal lobe containing green chlorophyll and a slightly larger thin, colourless, floating ventral lobe. Under some conditions, an anthocyanin pigment gives the fern a reddish-brown colour. Plant diameter ranges from 1-2.5 cm for small species such as Azolla pinnata, to 15 cm or more for Azolla nilotica. Azolla plants are triangular or polygonal in shape, and float on the surface of the water, individually or in mats. They give the appearance of a dark green to reddish carpet, except Azolla nilotica that does not produce the red anthocyanin pigment. The most remarkable characteristic of azolla is its symbiotic relationship with the nitrogen-fixing blue-green alga (cyanobacterium) Anabaena azollae. The fern provides nutrients and a protective cavity in each leaf to Anabaena colonies in exchange for fixed atmospheric nitrogen and possibly other growth-promoting substances (Lumpkin et al., 1980).

Azolla has a historical role in agriculture. For centuries, it has been recognized as a useful plant in Southern China and Northern Vietnam, where it has been used as a biofertilizer and green manure for the rice crop due to its N-fixing abilities (Van Hove et al., 1996). Azolla was also mentioned as a poultry feed in Peru in the 18^th century (Feuillée, 1725). Azolla production was heavily promoted in the early 1960s in China and Vietnam, resulting in a rapid expansion in these countries. It attracted international attention in the 1970s as a result of the oil crisis and the rising prices of fossil fuel-dependent N fertilizers. Azolla became a potential replacement for these as it was believed that it could bolster rice production in many tropical countries. However, enthusiasm for azolla faded in the 1980s and was followed by a period of scepticism. Azolla production in China and Vietnam declined (perhaps due to the increasing use of land for food production) and azolla development worldwide did not live up to initial expectations, due to serious constraints such as water availability, difficulties in maintenance and handling, high labour requirements and limited knowledge on the specific needs of each azolla species (Van Hove et al., 1996). For instance, adoption of azolla as a livestock feed failed in the Philippines (APO, 1990). It should be noted that azolla is often considered by farmers as a noxious weed, so perception of azolla is not always positive (Lumpkin et al., 1980).

However, azolla does have several unquestionable agronomic qualities: the capacity to fix atmospheric nitrogen, a very high productivity in the right environment, a high protein content, an herbicide effect and the capacity to decrease N-fertilizer volatilization. For those reasons, azolla started to attract attention again in the late 1990s, notably as a component of integrated farming such as rice-fish-azolla, rice-duck-azolla, rice-duck-fish-azolla or pig-fish-azolla systems (Van Hove et al., 1996). Adoption of azolla by livestock farmers still faces important hurdles. In India, for example, in spite of being promoted by non-government organizations, cooperatives and government agencies, adoption has been slow and sporadic due to poor yields, pests, handling and storage difficulties, and labour requirements (Chander, 2011; Tamizhkumaran et al., 2012).

Research and promotion of azolla as a livestock feed has been increasing. Because azolla has a higher protein content (19-30%) than most green forage crops and aquatic macrophytes, and an essential amino acid composition (notably lysine) favourable for animal nutrition, azolla can be a valuable protein supplement for many species, including ruminants, poultry, pigs and fish (Hasan et al., 2009).

Distribution

Azolla occurs in ponds, ditches and rice fields of warm-temperate and tropical regions throughout the world. Each species has a specific native range: Azolla caroliniana, Eastern North America and the Caribbean; Azolla filiculoides, Southern South America through Western North America including Alaska; Azolla microphylla, tropical and subtropical America; Azolla mexicana, Northern South America through Western North America; Azolla nilotica, upper reaches of the Nile to Sudan; Azolla pinnata, most of Asia and the coast of tropical Africa. These species have been dispersed by man and can be found outside their native regions (Lumpkin et al., 1980).

Water is the fundamental requirement for the growth and multiplication of Azolla as the plant is extremely sensitive to lack of water. Although Azolla can grow on wet mud surfaces or wet pit litters, it prefers a free-floating state. Azolla can survive within a pH range of 3.5 to 10, but optimum growth is observed in the range of 4.5 to 7. Optimum temperature for growth and nitrogen fixation depend on the species. It is usually in the 20-30°C range, though Azolla mexicana is more tolerant of temperatures over 30°C. Outside this range, growth decreases until the plant begins to die at temperatures below 5°C and above 45°C. Azolla filiculoides can withstand temperatures as low as -5°C without apparent harm. Saline tolerance depends on the species. The growth rate of Azolla pinnata was found to decline as salinity increased above 380 mg/l. At about 1.3% salt (33% of sea water) the growth of Azolla caroliniana ceased and higher concentrations resulted in death. Azolla filiculoides has been reported to be most salt-tolerant. During periods of stress, anthocyanin is thought to protect the photosynthetic apparatus from damaging high light intensities by absorbing some of the light and converting it to heat. For that reason, azolla often exhibits a red colour under field conditions, especially where phosphorus is deficient. Azolla grows best in full to partial shade (25-50% of full sunlight). Growth decreases quickly under heavy shade (lower than 1500 lux) and more than 50% of full sunlight reduces photosynthesis. The optimum relative humidity for azolla growth is between 85 and 90%. Azolla becomes dry and fragile at a relative humidity lower than 60% (Hasan et al., 2009; Lumpkin et al., 1980). Successful cultivation of azolla requires the application of a certain amount of phosphorus fertilizer (0.5 to 1.0 kg P/ha/week), but this does not necessarily mean an increase in the amount of phosphorus fertilizer required to produce a crop of rice (Lumpkin et al., 1985).

Processes

Azolla can be fed to livestock either in a fresh or dried form. It can be given directly or mixed with concentrates to cattle, poultry, sheep, goats, pigs and rabbits. It takes a few days for the animals to get used to the taste of azolla, therefore it is better to feed it with the concentrates in the initial stages. When dung is used as fertilizer in backyard azolla ponds, the azolla should be washed thoroughly with fresh water to remove the smell of the dung (Giridhar et al., 2013).

As fresh azolla is highly perishable, it is advisable to dry it immediately when there is a surplus, or for livestock species for whom a dried form is more practical or preferable. Azolla is usually dried in the shade and stored dry, for example in a plastic bin, for later use (Giridhar et al., 2013).

Forage management

Yield

Azolla is a highly productive plant. It doubles its biomass in 3-10 days, depending on conditions, and yield can reach 8-10 t fresh matter/ha in Asian rice fields. In India, yields of 37.8 t fresh weight/ha (2.78 t DM/ha) have been reported for Azolla pinnata (Hasan et al., 2009).

Azolla production

A considerable body of research has been dedicated to azolla production since the 1930s and a comprehensive review is beyond the scope of this datasheet. Azolla grows throughout the world, from temperate to tropical countries. Production methods must be adapted to local conditions and are not directly transferable from one country to another at a local level. Azolla production can be relatively inexpensive but is usually labour-intensive and requires proper training, otherwise the results can be disappointing (Lumpkin et al., 1985). Environmental constraints such as very high temperatures, low humidity, limited water availability and poor quality of water can restrict the adoption of azolla production (Giridhar et al., 2013).

Production for biofertilization

Production of azolla for green manure is done according to 3 systems. It can be grown as a monocrop and then incorporated as foundation manure before the rice is transplanted, or transported to another site for use on upland crops. Monocrop azolla has been used in China and Vietnam during winter and spring to produce nitrogen for the spring rice crop. Azolla can also be grown as an intercrop, and used as a top dressing manure after the rice is transplanted. This is done in places where there is no time available in the cropping system for growing azolla as a monocrop. It can also be grown both as a monocrop and an intercrop. This technique is designed to grow azolla before planting the rice crop, allowing production of added nitrogen for the crop through cultivation of intercropped azolla (Lumpkin et al., 1985).

Production of azolla for livestock feeding

A method for growing azolla for smallholder dairy farming in India has been described as follows. The farmer should select a shaded pond close to the house (to ensure regular upkeep and monitoring) and to a water source. An area of 4-4.5 m² and 10-15 cm deep can produce about 2 kg/d of fresh azolla, enough to supplement 2 dairy cows. A plastic sheet should be spread in the pond and properly secured. To initiate azolla growth, sieved fertile soil mixed with cow dung and water (or biogas slurry) should be added as fertilizer and the pond should be inoculated with fresh azolla culture (about 800 g for a 2 m² pond). The crop is maintained by application of about 1 kg of cow dung and 80-100 grams of superphosphate every 2 weeks. The first crop should be ready in 15-20 days and can then be harvested daily. The pond needs to be emptied once in six months. Azolla produced in excess should be dried in the shade for later use (Giridhar et al., 2013).

Environmental impact

Weed

Because azolla can form dense mats on water surfaces, it is classified as a water weed in many areas. It has been reported to disrupt fishing, access to water by livestock, impede water flow in ditches, clog pipes, pumps and floodgates and interfere with watercress cultivation (Lumpkin et al., 1980).

Environmental benefits

N-fixation and green manure

The main reason for the enduring popularity of azolla among agriculturists is its ability to fix nitrogen, valuable in paddy fields under waterlogged or flooded conditions where N-fixating legumes cannot grow. It is also a source of green manure for upland rice growing on the most fertile soils that farmers are reluctant to use for legume crops. In 25 to 35 days azolla can easily fix enough nitrogen for a 4 to 6 ton/ha rice crop during the rainy season, or a 5 to 8 ton/ha crop under irrigation during the dry season. Azolla also contributes to maintaining soil fertility, by providing nutrient-rich humus through its decomposition (Lumpkin et al., 1985).

Limitation of N volatilization

By reducing light intensity underwater, azolla inhibits algae photosynthesis and the subsequent increase in pH and NH₃ volatilization. Because up to 50% of N fertilizer applied to paddy fields is lost in volatilization, azolla could help to reduce the amount of N fertilizers in rice crops (Van Hove et al., 1996).

Weed control

It has been empirically observed, and well appreciated by rice farmers, that azolla suppresses the growth of some aquatic weeds by forming a thick mat that deprives weed seedlings of sunlight while mechanically preventing them from emerging (Lumpkin et al., 1985; Van Hove et al., 1996).

Mosquito control

The ability of azolla to prevent mosquito breeding and thus the spread of paludism was suggested in the early 20^th century (hence the name "mosquito fern") but was demonstrated only in the late 1980s by Indian and Chinese researchers. For example a Chinese experiment in controlled conditions showed that full or 2/3 azolla cover could prevent or limit the oviposition of Culex mosquitoes. It did not prevent ovipositing of Anopheles sinensis but limited the emergence of adult insects (Lu BaoLin, 1988). These findings were later confirmed in field trials that showed that larval density was greatly reduced when 75% of the water surface was covered by azolla (Lu BaoLin et al., 1989). However, there are some doubts about the efficiency of azolla in mosquito control, since the coverage required for a significant reduction in mosquito populations may be impossible to obtain in practice (Van Hove et al., 1996).

Bioremediation

Azolla can accumulate excessive amounts of pollutants such as heavy metals, radionuclides, dyes, pesticides, etc. For that reason, it has been extensively studied and tested since the 2000s as a candidate for the bioremediation of waste waters and effluents (see the review of Sood et al., 2012).

Other environmental benefits

Other benefits cited in the literature include the reclamation of saline soils and the production of biogas and bioenergy (Raja et al., 2012).

Integrated farming systems

Numerous integrated farming systems have been designed where combinations of azolla, rice (or another crop), fish, ducks and pigs can complement each other (see the Fish section on the "Nutritional aspects" tab).

Nutritional aspects

Nutritional attributes

The chemical composition of azolla species varies with ecotypes and with the ecological conditions and the phase of growth. The DM content is generally low, in the 5-7% range. The protein content is in the 19-30% DM range in optimum growth conditions. The amino acid profile of azolla depends on the species, but the lysine content is relatively high (4-6% of the protein). Unlike duckweeds, azolla is relatively rich in fibre: NDF can be higher than 50% DM, crude fibre is about 15% DM and the lignin content is in the 10-13% DM range. Like most aquatic plants, azolla is rich in mineral matter (10-20% DM) and can be used as a source of macro and micro minerals. However, the high fibre and high mineral contents explain why azolla should be generally included in limited amounts in the diets of monogastrics, as high inclusion rates tend to decrease performance. The bulkiness of fresh azolla is another limitation to its use in livestock diets and it is often preferable to dry it.

Potential constraints

Moisture

Fresh azolla is mostly composed of water, which makes it very bulky and difficult to transport, store and market (Huggins, 2007). It spoils in less than 48 hours in tropical conditions (Kumar, 2011) although it may have a shelf life of 7 days in colder climates (Huggins, 2007). This is one of the reasons for the poor adoption of azolla as a livestock feed in tropical countries (Chander, 2011).

Presence of fresh water shrimps

In a feasibility study in Australia, it was found that while the sampled azolla was clear of pesticides (organophosphates and organochlorides) and mycotoxins, it contained significant amounts of fresh water shrimps. Not only could the decomposing shrimps reduced palatability, but the presence of animals made the product illegal to feed to ruminants under the current Australian law (Huggins, 2007).

Minerals and contaminants

Azolla is a bioaccumulator and is naturally rich in minerals. While quantities of trace elements and heavy metals are unlikely to reach toxic levels in farmed azolla, azolla used for bioremediation should not be fed to animals (Leterme et al., 2009). For instance, the lead content of Azolla filiculoides grown in water treated with 20 mg/l/d of lead for 6 days reached 2.3% DM (Oren Benaroya et al., 2004).

Ruminants

Azolla, fresh and dried, can be used in the diets of cattle, sheep and goats. In spite of the long recorded utilization of azolla in ruminants, data are still scarce. Trials in India indicate that fresh or dried azolla can be a partial substitute to more conventional sources of protein such as groundnut meal.

Nutritive value

The estimated energy value (gas production method) of azolla for ruminants is moderate (ME 7.4 MJ/kg DM) though in vitro DM digestibility is high (80%) (Parashuramulu et al., 2013). In a sheep trial, the OM, protein and fibre digestibilities of diets where dried azolla replaced 30% of groundnut meal were higher than that of the control diet, but DM intake was lower (Reddy et al., 2011). Lower DM and protein digestibilities and higher intakes were found in another experiments with 10 or 20% dried azolla in the diet (Wadhwani et al., 2010). On the basis of an in vitro analysis (Rumen Simulation Technique, RUSITEC), it was concluded that Azolla pinnata could be used as a protein supplement by replacing 30% of the protein content in ruminant diets (Ahirwar et al., 2009).

Feeding trials

Most of the feeding trials with azolla in dairy cattle (cows and buffaloes), growing buffaloes, sheep and goats have been carried out in India. Since the year 2000, azolla has been promoted in India for dairy production (Pillai et al., 2004). In a project for the development of disadvantaged areas of Bidar District (India), azolla production for increasing output from dairying was found to have the second highest benefit:cost ratio after production of worms for vermicomposting (Desmukh et al., 2013).

All trials summarized in the table below took place in India with Azolla pinnata.

Animal	Trial	Results	Reference
Crossbred cows, mid-lactation	2 kg/d fresh azolla replacing 50% of concentrate for 3 months	Azolla maintained dairy performance while decreasing feed+labour costs by 16.5% and milk production costs by 18.5%.	Murthy et al., 2013
Dairy buffaloes	Napier grass/rice straw/rice bran diet supplemented either with 1 kg sesame meal or 1.5 kg fresh azolla for 120 d	Higher milk yield and milk fat with the supplemented diets. Azolla can substitute for sesame meal.	Kumar, 2008
Murrah buffalo bulls, 310 kg	Sun-dried azolla replaced 25% of the protein in the concentrate (azolla 225 g/d)	Azolla decreased nutrient digestibility but its inclusion reduced the feed cost.	Kumar et al., 2012
Buffalo calves	50% of groundnut meal protein was replaced by (fresh) azolla protein	Azolla increased daily gains (294 vs. 240 g/d) and feed efficiency, and reduced feed costs.	Indira et al., 2009
Adult Nellore sheep, 12-14 months	Replacement of 30% of groundnut meal with dried azolla	Better nutrient digestibility but lower intake.	Ghodake et al., 2012
Marwari, Patanwadi and Merino × Patanwadi weaner lambs, 4 months	Utilization of non-conventional ingredients including sun-dried azolla at 10 and 20% in the diets	Lower DM and protein digestibilities but higher DM and protein intakes. Azolla had no effect on carcass traits. Feed costs were lower.	Wadhwani et al., 2010.
Osmanabadi goat kids, 3 months	Replacement of the concentrate with 15 or 25% dried azolla	Inclusion of dried azolla up to 15% increased performance though it depressed nutrient digestibility.	Ghodake et al., 2012
Black Bengal goats	Replacement of the concentrate with up to 50% sun-dried azolla	Inclusion of dried azolla up to 20% maintained growth with no adverse effect. A 50% inclusion rate resulted in profuse diarrhoea.	Tamang et al., 1993

Pigs

Azolla has been used to feed pigs in South-East Asia, including Vietnam, Singapore and Taiwan (Chander, 2011), and it has been tested in other tropical and subtropical countries. It can be generally considered as a good source of minerals and essential amino acids but its interest is limited in pig production due to its low digestible energy (10.8 MJ/kg DM) and digestible protein. Azolla should not account for more than 10-15% of the total intake in growing pigs as higher inclusion rates tend to depress performance. Due to the high water content of fresh azolla and, therefore, its bulkiness, higher intake levels are likely to be unachievable (Leterme et al., 2009). In Vietnam, azolla has been used as a sole feed for lactating sows, which have a higher intake and are able to deal with the low DM content (Chander, 2011).

Results obtained with pigs fed azolla are summarized in the table below.

Country	Pig type	Azolla species	Trial	Results	Reference
Colombia	PIC Andina, growing pigs, 55-60 kg	Azolla filiculoides	Dried and ground azolla fed at 12.5 or 25% of the diet	Azolla has a low digestible energy and its inclusion in the diet decreased amino acid digestibility. Inclusion rate should not exceed 10-15% DM.	Leterme et al., 2009
Colombia	PIC Andina, gilts, 110 kg	Azolla filiculoides	In addition to a basal diet, the sows were fed 80-90 g/kg W^0.75 fresh or dry azolla-based diets	Inclusion of azolla decreased amino acid availability in the diet. Sows were able to ingest up to 1.2 kg DM of azolla per day when it was offered dried and ground (which represents 9 kg of fresh azolla), but only 0.6 kg/day if fresh.	Leterme et al., 2010
Vietnam	Growing pigs	Azolla sp.	Azolla replaced 50% of the rice bran	Reduced performance in the growing phase but faster growth in the period from 24 to 89 kg.	Cited by Chander, 2011
China	Growing pigs	Azolla sp.	Fresh azolla replaced part of the concentrate	Growing pigs fed azolla gained 26.2 g/day and starter pigs 28.4 g/day more than those fed only concentrate. 97.4 kg of fresh azolla produced 1 kg of live weight gain.	Zhang ZhuangTa et al., 1987
Bénin	Local piglets, 17 kg	Azolla microphylla	Fresh azolla fed at 15, 30 and 45% in the diet (fresh basis)	15% resulted in the highest performance and least feed cost. The 30 and 45% rates were detrimental to performance and feed efficiency, due to a nutrient imbalance associated with feeding a high-moisture and bulky product.	Accodji et al., 2009
Venezuela	Landrace x Yorkshire growing pigs, 25 kg	Azolla sp.	Soybean meal, fresh sugarcane juice, palm oil and fresh azolla (16% of diet DM) supplemented or not with fish meal	Pig consumed up to 4.8 kg/d of fresh azolla.	Pinto-Santini et al., 2005
India	Desi pigs	Azolla sp.	Sun-dried azolla fed at 10, 20 and 30% of the diet	Best daily gain occurred with azolla included at 10%. A 30% inclusion rate depressed feed efficiency	Parthasarathy et al., 2003
Philippines	Hypor growing pigs, 5-week old	Azolla sp.	Diet containing 20 or 40% dried azolla + commercial feed, fed ad libitum	Performance decreased with increasing rate of azolla but a 20% rate was acceptable.	Gavina, 1994
Colombia	Growing pigs	Azolla filiculoides	Basal diet plus a protein supplement and 2.6 kg or 5.2 kg of fresh azolla	In the growing phase, pig performance decreased as the inclusion of azolla increased. The effect was reversed in the finishing phase, pigs fed azolla grew faster than on the control diet.	Becerra et al., 1990
Philippines	Weanling and growing pigs	Azolla sp.	Azolla meal fed at 5, 10 or 15% replacing rice bran	Best daily gain was obtained in weaners when azolla was included at 10%. In grower diets, feed conversion efficiency was similar to that of the control at 20% azolla meal in the diet.	Alcantara et al., 1989

Poultry

Azolla has been used in numerous trials, notably in Asia, as a feed for broilers, village chickens, laying hens and grazing ducks in rice fields where azolla is used as a N fertilizer.

Broilers and pullets

There is a general consensus that dried azolla in broiler diets should be limited to 5% as higher levels tend to depress nutrient utilization and performance (Parthasarathy et al., 2002; Basak et al., 2002). In pullet chicks, azolla could be included safely at up to 10% (Alalade et al., 2006). Fresh azolla could replace 20% or more of a commercial broiler diet (Subudhi et al., 1978; Namra et al., 2010).

Country	Poultry type	Azolla species	Trial	Results	Reference
India	Broilers	Azolla sp.	0 to 20% dried azolla in the diet	Azolla at 10-20% depressed growth and protein efficiency ratio but had no effect on survivability. Azolla at 5% resulted in satisfactory growth.	Parthasarathy et al., 2002
Bangladesh	Vencobb broilers from 7 to 42 d	Azolla pinnata	0 to 15% dried azolla in the diet	Azolla included at 5% improved live weight, feed conversion ratio, protein and energy efficiency, dressing percentage and profitability. Higher inclusion rates depressed performance.	Basak et al., 2002
Nigeria	Nera brown pullets, 2 weeks	Azolla pinnata	0 to 15% dried azolla in the diet	Azolla fed at up to 10% gave the best performance.	Alalade et al., 2006
Egypt	Fayoumi broilers, 2 to 16 weeks	Azolla sp.	Commercial feeds offered at 15-45% of restricted diets, supplemented with fresh azolla given ad libitum	Though performance and slaughtering parameters decreased with increasing restriction rates, optimum economical efficiency was obtained with the group fed fresh azolla ad libitum supplementing the diet restricted at 45%.	Namra et al., 2010
India	Vencobb broilers, 1 to 42 d	Azolla hybrid Rong-Ping	0 to 10% dried azolla in the diet	Performance was maintained up to 7.5% inclusion rate.	Prabina et al., 2010
India	Broilers, 160 d	Azolla pinnata	0 to 4.5% sun-dried azolla in the diet	4.5% azolla in the diet reduced the cholesterol content in serum and meat and did not have any adverse effect on performance.	Balaji et al., 2009; Balaji et al., 2010
India	Broilers, 225 d	Azolla sp.	0 to 5% dried azolla partially replacing soybean meal	Replacement of soybean meal by dried azolla up to 5% had no deleterious effects on palatability, efficiency of feed utilization and carcass quality, and was profitable.	Dhumal et al., 2009
Bangladesh	Broilers, 1-14 d	Azolla pinnata	10% dried azolla partially replacing maize and soybean meal	10% dried azolla could replace maize and soybean meal on an equal digestible protein basis in broiler diets.	Ali et al., 1995
India	White Leghorn chicken, 5 weeks	Azolla pinnata	20% dried azolla in the diet	Inclusion of fresh Azolla in the diet can replace about 20% of commercial feed.	Subudhi et al., 1978

Smallholder chicken production

Azolla has been proposed as a way to make smallholder poultry production more profitable by reducing feed costs, notably in impoverished areas. A study in 42 villages in the northern plains of Uttar Pradesh (India) showed that rural poultry integrated with azolla cultivation was able to provide sustainable livelihood security as well as income (Rai et al., 2012).

Country	Poultry type	Azolla species	Trial	Results	Reference
Andaman Islands	Nicobari chickens, 42 d	Azola pinnata	Fresh azolla at 200 g/d + 120 g/d basal diet, for 45-60 weeks vs. basal diet alone	Higher final weight, growth and feed conversion ratio with azolla, no effect on egg production and immunocompetence. Azolla supplementation was profitable due to savings on feed cost.	Sujatha et al., 2013a
India	Nirbhik chickens (dual purpose), Shyama chickens (egg)	Azola pinnata	Azolla grazed ad libitum	Chickens fed azolla had a higher body weight at 8 weeks or higher egg production after 40 and 72 days than chickens not supplemented with azolla.	Rai et al., 2012

Laying hens

Trials in India and Nigeria showed that dried azolla can be used at up to 15% of the diet for laying hens (Alalade et al., 2007; Khatun et al., 2008). Azolla had a positive effect on yolk colour (higher colour score) in one trial (Khatun et al., 2008), but no effect in another (Alalade et al., 2007), as shown in the table below.

Country	Poultry type	Azolla species	Trial	Results	Reference
India	Commercial hens, 16 week trial	Azolla sp.	0 to 20% dried azolla in the diet	Azolla meal could be considered as a source of protein and pigment without any harmful effects on production performance up to 15%.	Khatun et al., 2008
Nigeria	Nera brown hens	Azolla pinnata	0 to 15% sun-dried azolla in the diet	Azolla fed up to 15% did not affect hen-day production and egg quality to 30 weeks, but resulted in lower yolk weight.	Alalade et al., 2007

Ducks

Fish, azolla and ducks integrated with a rice farming system can result in better nutrient recycling, pest control (weed, insects, golden apple snail), feed supplementation and higher productivity (Cagauan et al., 2000). While azolla in such systems principally serves as a nitrogen fertilizer for the rice crop, it can also be fed directly to the ducks as a protein supplement.

Country	Poultry type	Azolla species	Trial	Results	Reference
Andaman Islands, Nicobar Islands	Native laying ducks, 20 weeks	Azolla pinnata	Fresh azolla at 200 g/d + layer mash, 20-33 weeks vs. layer mash alone	No effect of azolla on hen-day egg production and other performance parameters but much lower feed intake and higher fan colour score. Azolla supplementation was profitable due to savings on feed cost.	Sujatha et al., 2013b
Japan	Ducklings, 2 to 8 weeks	Mixture of 5 azolla species	Fresh azolla supplementing a formula feed	Ducklings fed azolla had greater growth rates than birds fed the control diet.	Liu Xiang et al., 1998
Philippines	Native ducks	Azolla sp.	Fresh azolla + 40 or 60% chicken grower mash	Fresh azolla was detrimental to growth performance.	Gavina, 1994
Philippines	Mallard ducks	Azolla microphylla	Partial replacement (20%) of a rice grain-snail-shrimp diet	Similar egg production and intensified yolk colour.	Alejar et al., 1989

Other birds

Japanese quails (Coturnix coturnix japonica)

In India, azolla (Azolla pinnata) was found to have potential as a cheap, safe and high density nutrient-rich feed for quails, but inclusion rates higher than 5% depressed growth performance and feed conversion (Sujatha et al., 2013b).

Geese

In China, azolla has been used as a green forage for geese. The daily weight gain of geese fed azolla was close to that of geese fed vegetables (Zhang ZhuangTa et al., 1987).

Rabbits

Azolla appears to be a suitable feed for rabbits. In one trial, where 6-week old rabbits were given diets containing 0 to 36% dried azolla, it was concluded that growing rabbits can be safely fed rations containing 24% dried azolla hay resulting in beneficial effects on most production traits (Abou-Zeid et al., 2001). In another trial with female breeding rabbits, replacing 25% of soybean meal protein by protein from sun-dried azolla maintained feed conversion, litter size at weaning and female weight, as well as economic performance. However, conception rate, litter size at birth and milk production were depressed (Sabra et al., 2006).

Fish

There have been numerous aquaria or field trials on the benefits of azolla for fish culture. The literature up to 2008 has been reviewed by Hasan et al., 2009.

Palatability

Preference studies carried out in aquaria indicate that cichlids (Oreochromis, Tilapia and Cichlasoma) as well as a grass carp x bighead carp hybrid tend to prefer Azolla caroliniana (Antoine et al., 1986; Lahser, 1967; Fiogbé et al., 2004; Micha et al., 1988).

Performance

Growth studies have been carried out under laboratory rearing conditions with fresh or dried azolla.

Cichlids

Most of azolla experiments on cichlids have been negative. Fish died or negative growth was recorded when fed exclusively with fresh azolla (Hasan et al., 2009). In Nile tilapia fingerlings (Oreochromis niloticus), feeding azolla fresh, powdered or pelleted, replacing 10 to 90% of the control diet was detrimental to all performance parameters. Adult tilapia fed azolla ad libitum, fresh or pelleted, suffered weight loss in a 30-day feeding trial (Almazan et al., 1986). Poor growth and feed utilization were also reported with Oreochromis niloticus, Cichlasoma melanurum and Tilapia rendalli fed Azolla microphylla-based diets (Antoine et al., 1986; Micha et al., 1988). Nile tilapia fingerlings and adults fed Azolla pinnata as a fish meal replacer at substitution levels of 25-100% performed extremely poorly even at the lowest level (El-Sayed, 1992). In contrast, between 30 and 42% of fish meal-based diets fed to Nile tilapia have been successfully replaced by azolla meal without negatively affecting fish performance (Santiago et al., 1988; Naegel, 1997). In Nile tilapia fed up to 50% dried Azolla filiculoides in concrete tanks or in earthen ponds, fish grown in tanks performed less well than fish grown in ponds, due to the presence of natural feeds in the ponds. The fish fed in ponds also had a more valuable fatty acid profile (lower n-3:n-6 ratio) (Abou et al., 2013). The poor growth of cichlid fish fed diets containing higher levels of azolla may be due to excesses or deficiencies of amino acids (Fiogbé et al., 2004).

Cyprinids

In a comparison between alfalfa, duckweed (Lemna sp.) and Azolla filiculoides fed fresh to grass carp (Ctenopharyngodon idella) at 20% BW (plus a formulated diet), azolla gave the lowest growth rates (Nekoubin et al., 2013). In rohu (Labeo rohita) fed a dried mixture of Azolla microphylla and Azolla pinnata incorporated in the diet at 15%, 25% and 35%, fish fed the 25% azolla diet had the highest growth rate and resulted in a lower fat content in the fish (Datta et al., 2011).

Integrated systems

Rice-fish-azolla systems

Azolla has been increasingly used as feed and/or fertilizer in studies with rice-fish culture systems in many Asian countries. One of the most successful uses of azolla is its use as fertilizer and/or feed in an integrated rice-fish-Azolla system, which allows the simultaneous development of rice, azolla and different fish species (planktophages, macrophytophages and polyphages). Each of the partners contributes to the equilibrium of the system. The fish derive a benefit from azolla, depending on the species. Fish waste promotes the proliferation of plankton that is consumed by some of the fish and fertilizes the rice. The polyphagous fish protect rice and azolla from a number of insects and molluscan pests. It is necessary to maintain equilibrium between the population of fish and that of azolla, either by introducing a supplementary biomass of azolla collected elsewhere, or by harvesting the excess biomass (Van Hove, 1989; Hasan et al., 2009). Several comparisons between rice-fish-azolla system and rice-fish cultivation alone have shown the potential benefits in terms of fish yields (Indian carp, tilapia) of such integrated systems in India and in the Philippines (Cagauan et al., 1991; Hasan et al., 2009).

Fish-azolla systems

In India, finely chopped Azolla caroliniana placed in a feeding basket under pond conditions was found to be a preferred feed for grass carp fingerlings (Ctenopharyngodon idella), with the final weight gain of azolla-fed fish being significantly higher than those on the control diet (Majhi et al., 2006). In a semi-intensive carp polyculture system, diets containing 10 to 40% dried azolla had no significant affect on the water quality, except for the nitrate-nitrogen content. All fish species recorded significantly higher growth with diets containing up to 20% azolla (Dhawan et al., 2010). In a duck-fish-azolla integrated system in the Philippines, Nile tilapia, stocked in ponds fertilized with a mixture of fresh pig and duck manure, could eat all the azolla every 6 or 7 days (Gavina, 1994). Weight gain comparisons of azolla-fed fish were carried out in China using grass carp, Nile tilapia, crucian carp (Carassius carassius) and silver carp (Hypophthalmichthys molitrix). Grass carp, Nile tilapia and crucian carp gained weight but azolla was detrimental to the growth of silver carp (Cagauan et al., 1991).

Nutritional tables

Tables of chemical composition and nutritional value

Avg: average or predicted value; SD: standard deviation; Min: minimum value; Max: maximum value; Nb: number of values (samples) used

Azolla (Azolla spp.), fresh

Includes different azolla species

Main analysis	Unit	Avg	SD	Min	Max	Nb
Dry matter	% as fed	6.7	1.3	5.1	8.7	8
Crude protein	% DM	20.6	3.5	13.9	28.1	15
Crude fibre	% DM	15.0	3.5	11.3	22.8	9
NDF	% DM	43.8	5.9	35.4	52.3	6
ADF	% DM	31.8	6.4	24.0	38.9	5
Lignin	% DM	11.4	1.7	9.3	13.5	5
Ether extract	% DM	3.8	1.3	1.9	5.1	9
Ash	% DM	15.9	3.5	9.8	21.6	12
Starch (polarimetry)	% DM	4.1		2.7	5.5	2
Gross energy	MJ/kg DM	17.0					*

Minerals	Unit	Avg	SD	Min	Max	Nb
Calcium	g/kg DM	11.0	4.1	5.8	17.0	8
Phosphorus	g/kg DM	6.1	5.5	0.3	15.5	11
Potassium	g/kg DM	17.4	3.7	10.9	22.5	7
Sodium	g/kg DM	9.0	4.3	2.8	12.5	4
Magnesium	g/kg DM	5.0	0.8	3.9	6.1	5
Manganese	mg/kg DM	762	438	208	1429	5
Zinc	mg/kg DM	38	28	11	77	5
Copper	mg/kg DM	16	7	10	28	5
Iron	mg/kg DM	3900	3794	711	8200	5

Amino acids	Unit	Avg	SD	Min	Max	Nb
Alanine	% protein	6.4	1.0	5.3	7.4	3
Arginine	% protein	5.9	0.7	5.1	6.6	3
Aspartic acid	% protein	9.3	1.0	8.2	10.3	3
Cystine	% protein	1.6	0.8	0.7	2.3	3
Glutamic acid	% protein	12.6	1.0	11.6	13.5	3
Glycine	% protein	5.6	1.1	4.5	6.6	3
Histidine	% protein	2.1	0.4	1.6	2.4	3
Isoleucine	% protein	4.5	0.8	3.7	5.4	3
Leucine	% protein	8.4	1.2	7.0	9.2	3
Lysine	% protein	4.7	1.1	3.5	6.5	5
Methionine	% protein	1.4	0.3	1.2	1.9	5
Phenylalanine	% protein	5.4	0.2	5.2	5.6	3
Proline	% protein	4.9	1.7	3.5	6.8	3
Serine	% protein	4.5	0.9	3.9	5.6	3
Threonine	% protein	4.7	0.7	4.0	5.3	3
Tryptophan	% protein	1.8		1.5	2.0	2
Tyrosine	% protein	3.6	0.5	3.2	4.1	3
Valine	% protein	5.5	1.5	3.8	6.8	3

Ruminant nutritive values	Unit	Avg	SD	Min	Max	Nb
OM digestibility, ruminants (gas production)	%	64				1
ME ruminants (gas production)	MJ/kg DM	7.4				1

Pig nutritive values	Unit	Avg	SD	Min	Max	Nb
Energy digestibility, growing pig	%	63.4				1
DE growing pig	MJ/kg DM	10.4				1

The asterisk * indicates that the average value was obtained by an equation.

References

AFZ, 2011; Becerra et al., 1990; Buckingham et al., 1978; CIRAD, 1991; Huggins, 2007; Leterme et al., 2009; Ly et al., 2002; Malek et al., 2008; Murthy et al., 2013; Parashuramulu et al., 2013; Pozy et al., 1996

Last updated on 13/12/2013 16:33:16

Azolla (Azolla spp.), dried

Includes different azolla species

Main analysis	Unit	Avg	SD	Min	Max	Nb
Dry matter	% as fed	91.9	1.9	88.6	94.9	8
Crude protein	% DM	21.5	5.3	10.7	31.8	18
Crude fibre	% DM	16.1	4.3	7.3	24.3	17
NDF	% DM	49.5	8.3	36.9	62.1	9
ADF	% DM	40.4	10.8	24.5	56.8	9
Lignin	% DM	8.9		4.5	13.2	2
Ether extract	% DM	3.3	0.9	1.6	5.2	16
Ash	% DM	19.2	5.8	11.0	36.1	18
Gross energy	MJ/kg DM	16.4					*

Minerals	Unit	Avg	SD	Min	Max	Nb
Calcium	g/kg DM	12.5	1.6	10.8	14.3	4
Phosphorus	g/kg DM	6.7	5.0	2.1	12.9	4
Potassium	g/kg DM	12.5				1
Sodium	g/kg DM	0.0				1
Magnesium	g/kg DM	3.5				1
Manganese	mg/kg DM	174				1
Zinc	mg/kg DM	88				1
Copper	mg/kg DM	17				1
Iron	mg/kg DM	756				1

Amino acids	Unit	Avg	SD	Min	Max	Nb
Alanine	% protein	5.8				1
Arginine	% protein	6.4	1.5	5.0	8.9	8
Aspartic acid	% protein	8.3				1
Cystine	% protein	0.9		0.8	0.9	2
Glutamic acid	% protein	9.6				1
Glycine	% protein	4.9		4.6	5.2	2
Histidine	% protein	1.6	0.4	1.2	2.2	7
Isoleucine	% protein	3.9	0.8	2.8	5.2	8
Leucine	% protein	8.7	1.4	7.4	11.4	8
Lysine	% protein	5.6	1.3	3.8	7.9	8
Methionine	% protein	1.5		1.5	1.6	2
Phenylalanine	% protein	4.7		4.6	4.7	2
Proline	% protein	4.0				1
Serine	% protein	4.1		4.0	4.2	2
Threonine	% protein	4.3	0.8	3.4	5.6	8
Tryptophan	% protein	1.2		0.5	1.8	2
Tyrosine	% protein	3.1		3.0	3.2	2
Valine	% protein	4.5	0.9	3.2	5.5	8

Poultry nutritive values	Unit	Avg	SD	Min	Max	Nb
AMEn broiler	MJ/kg DM	4.4				1

The asterisk * indicates that the average value was obtained by an equation.

References

Alalade et al., 2006; Ali et al., 1995; Basak et al., 2002; Datta et al., 2011; Domínguez et al., 1996; Gavina, 1994; Khatun et al., 1999; Kumar et al., 2012; Leterme et al., 2010; Naegel, 1997; Namra et al., 2010

Last updated on 13/12/2013 17:07:28

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Datasheet citation

Tran G., 2015. Azolla. Feedipedia, a programme by INRAE, CIRAD, AFZ and FAO. https://www.feedipedia.org/node/565 Last updated on October 19, 2015, 14:31

English correction by Tim Smith (Animal Science consultant) and Hélène Thiollet (AFZ)

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