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 <div class="title"><h3>4.28 - Azolla-Anabaena symbiosis in rice paddies</h3><br><h3 class="ch-owner">Matthew Paonessa, University of Guelph, Canada</h3></div>
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<p>Suggested citation for this chapter.</p>
<p>Paonessa,M. (2022) Azolla-Anabaena symbiosis in rice paddies. In Farmpedia, The Encyclopedia for Small Scale Farmers. Editor, M.N. Raizada, University of Guelph, Canada. http://www.farmpedia.org</p>
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       <h3 class="title-bg">Background</h3>
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<p><b>Azolla-Anabaena Symbiotic Relationship</b></p>
          <p>Azolla is a type of aquatic fern that floats and grows at the surface of water – it is the well known green layer that floats on the surface of rice paddies in Asia (Bhuvaneshwan and Singh, 2015). Although the practice of using Azolla in rice paddies is most prominent in eastern Asia, species of Azolla can be found on all continents, providing farmers the opportunity to incorporate the fern into their rice paddy crops (Carrapiço et al., 2000). It is naturally found in sources of freshwater such as ditches, lakes, and ponds and uses vegetative propagation (asexual reproduction without the use of spores or seeds) to reproduce (Azolla Foundation, 2016). The fern is extremely small and is one of the fastest growing plants on earth, having the potential to double the area it covers in 3 to 10 days (Hasan and Chakrabarti, 2009). Anabaena bacteria live within small oval pockets inside the Azolla leaves (Carrapiço et al., 2000). In exchange for this safe living environment, Anabaena bacteria provide a source of organic nitrogen to the Azolla ferns, allowing for the plant to rapidly reproduce. Anabaena is able to supply this organic nitrogen to the Azolla through a process called nitrogen fixation. Nitrogen fixation is when an organism has the ability to take nitrogen out of the atmosphere, which cannot be directly used by a plant, and change it into usable nitrogen. Consequently, the symbiotic relationship between Azolla and Anabaena generates a high concentration of nitrogen inside of the Azolla plant (Carrapiço et al., 2000).</p>
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       <h3 class="title-bg">Azolla Application</h3>
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          <p>The easiest way to incorporate Azolla into a new body of water is by taking a bucket full of Azolla from an area where Azolla naturally occurs, and throwing this bucket of water into an area that does not have any Azolla (Raizada and Smith, 2016) This concept is illustrated in the SAK picture book and a video demonstration by Indian farmers shows how easy it is to introduce Azolla into a new body of freshwater. They essentially release Azolla from a bag and leave it to reproduce (Azolla Philippines, 2013). Once the Azolla is introduced into the new water source it has the potential to begin to reproduce and cover the surface of the water. If Azolla cannot be found naturally it may be available for purchase from a local farmer who is cultivating it (Lumptkin, 1987). Online purchasing of Azolla may be made available soon in developing nations as it is now listed, but not in stock, on a number of plant websites supplying countries such as South Africa (Plants in Stock, 2015). The ideal temperature for Azolla is between 18˚C and 28˚C (Azolla Foundation, 2016). Some Azolla species are capable of surviving temperatures as low as -5˚C and as high as 35˚C. No species of Azolla can survive temperatures exceeding 45˚C (Azolla Foundation, 2016). Azolla grows the best in shallower rice fields of 5 cm or less as its roots grow closer to the soil, but the fern can grow to suitable levels in deeper waters (Talpur et al., 2013). Azolla grows best under partial sunlight as the light regulates photosynthesis and nitrogen fixation (Azolla Foundation, 2016). Azolla can grow in a source of water with a pH level of 3.5 to 10, but grows best in pH levels from 5.5 to 6.5. (Azolla Foundation, 2016).</p>
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       <h3 class="title-bg">Species of Azolla</h3>
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          <p>There are several different species of Azolla and they all facilitate the nitrogen producing symbiotic relationship with Anabaena. The different species are found across the world from China, to South America, to central Africa (Carrapiço et al, 2000). A. pinnata is a species of Azolla established in a number of continents, including Africa, which has been found to grow best under low levels of phosphorus compared to other species of Azolla (Watanabe and Liu, 1992). A. microphylla, common in the Galapagos Islands, is particularly in need of high phosphorus levels for optimization of its growth. At the same time A. microphylla has a highest resistance to heat, whereas, A. filiculoides, found throughout China, is the least heat resistant Azolla species (Watanabe and Liu, 1992).</p>
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       <h3 class="title-bg">Benefits of Azolla-Anabaena relationship to paddy rice yields</h3>
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 <p>-The symbiotic relationship between Azolla and Anabaena has led to Azolla being used as a bio-fertilizer, primarily used in rice paddy production (Azolla Foundation, 2016). Azolla is commonly grown within rice paddies, in the water directly alongside rice plants. Nitrogen is slightly leached into the water during Azolla's lifecycle (Azolla Foundation, 2016). When the rice plants near maturity, the canopy resulting from their leaves blocks sunlight from reaching the Azolla (Wagner, 1997). As a result the nutrients in the Azolla are depleted and the Azolla begins to rapidly decompose. It releases its fixed nitrogen into the water which rice plants can then absorb as they begin grain development (Wagner, 1997). This additional source of nitrogen is especially important for the growth of rice plants as a lack of nitrogen is the most limiting factor in rice production (Vaishampayan et al., 2001).

<p><b>Higher Rice Production Yields</b></p>
<p>Numerous studies have shown that growing Azolla alongside rice plants can increase rice yields from anywhere between 14-40% (Talley et al., 1977). Experiments have found that Azolla may slow the growth of rice plants in their early stages, mostly likely from competition for nutrients. Even so, as the rice plants reach maturity, a taller plant with more shoots is developed (Wagner, 1997). When Azolla is used on a rice paddy alongside synthetic fertilizer, farmers have seen yield gains as high as 73% (Carrapiço et al, 2000).</p>

<p><b>Reduced Input Costs</b></p>
<p>Using Azolla as a bio-fertilizer means that farmers will not have to spend as much money on purchasing synthetic fertilizers. Studies have shown that a single crop of Azolla provides the same level of nitrogen acquired from 30 kg N/ha of urea which contains the highest concentration of nitrogen in solid fertilizers (Watanabe, 1987). Azolla can also be used effectively with synthetic fertilizers such as urea. For instance 2 kg of Azolla used with 30k g N/ha of urea provide the same amount of nitrogen as 60 kg N/ha of urea (Watanabe, 1987). Azolla can produce as much as 2-3 kg of nitrogen per hectare, per day (Hasan and Chakrabarti, 2009).</p>

<p><b>Additional Benefits</b></p>
<p>Azolla can quickly cover the entire surface of a rice paddy due to its rapid rate of reproduction (Azolla Foundation, 2016). The surface cover of Azolla can prevent mosquitoes from reproducing as the Azolla has blocked off access to the water. The inhibiting of mosquito reproduction in turn limits exposure to potentially disease caring mosquitoes (Azolla Foundation, 2016). </p>

<p>The thick cover of Azolla also prevents weeds from growing in the rice paddy as sunlight is blocked, preventing photosynthesis from occurring (Azolla Foundation, 2016). The suppression of weeds can be seen as a major benefit of growing Azolla as woman spend a disproportionate amount of their time on the farm pulling weeds, preventing them from engaging in other forms of work (Foster and Rosenzweig, 1996). </p> 

<p>The use of Azolla as a natural fertilizer bypasses many of the negative impacts associated with synthetic fertilizers. Synthetic fertilizers are usually washed away in runoff from farmland and end up polluting aquatic ecosystems as well as leaching into groundwater (Wagner, 1997). Long-term use of synthetic nitrogen fertilizers causes the acidification of soils, greatly reducing the growth rate of plants. The production of synthetic fertilizers is another cause of pollution as the process is highly intensive (Wagner, 1997). </p>
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       <h3 class="title-bg">Problems Associated with Azolla Growth</h3>
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<p>Azolla cannot survive for more than a few days without the presence of water (Wagner, 1997). Once the Azolla fern is put under moisture stress, even in the slightest where the moisture content of the tissue decreases to 80%, Azolla nitrogen production changes to one fifth of the optimal nitrogen fixing level which requires 88-95% moisture tissue content. Azolla plants are also susceptible to insects such as moths, snails, flies, and fungal diseases especially in tropical, hot, and humid weather. Measures can be taken against these pests but they are usually costly (Wagner, 1997).</p> 

<p>In terms of nutritional needs, phosphorus is the most limiting for the Azolla plant (Wagner, 1997). Azolla does not grow directly from the soil and phosphorus has a low mobility which prevents it from being available in abundance in the water (Ludwick, 1998)). Farmers may have to purchase phosphorus fertilizers to promote Azolla growth if phosphorus levels are insufficient in the rice paddy water (Wagner, 1997). Although Azolla can be used effectively alongside synthetic nitrogen fertilizers, nitrogen levels in the water that are too high can limit nitrogen fixation of Anabaena and the growth rate of Azolla.</p>  

<p>Pesticides have a mild effect on Azolla depending on which pesticide is being used. For example Molinate reduces the nitrogen fixing levels of Anabaena but increases the level of chlorophyll whereas a different pesticide, Carbofuran, increased both chlorophyll and Anabaena nitrogen fixing levels (Wagner, 1997). The vast majority of herbicides are detrimental to Azolla-Anabaena life by either inhibiting their growth or by preventing photosynthesis from taking place (College of Tropical Agriculture and Human Resources, 2013). </p> 

<p>Regardless of the potential benefits of Azolla on crop yields, Azolla use as a natural fertilizer is fairly low across the world (Kollah et al.,2016). Many farmers are unaware of the potential benefits of Azolla and consider it a weed, pulling it out of their rice paddies. Other farmers continue to buy synthetic fertilizers as some are subsidized by their governments. Besides the subsidized price, farmers purchase these synthetic fertilizers in large part because they have not been taught about the potential benefits of Azolla-Anabaena (Kollah et al.,2016).</p> 
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       <h3 class="title-bg">Azolla in Practice</h3>
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<p>Although Azolla is most commonly associated with eastern Asia, species of Azolla can be found across the world. Azolla experiments in Guinea-Bissau have had positive results. Azolla can be found in abundance in Guinea-Bissau's eastern river systems (Carrapiço et al., 2000). After a number of trials a mixture of Azolla and urea was found to have a yield increase of 73% compared to the control, and only 20% less of an increase from the highest yield using only urea, but at half the cost due to the incorporation of Azolla. In a mainly agrarian country where synthetic fertilizer prices hold great influence over a farmer's ability to produce crops, Azolla has the potential to give farmers more freedom with their income as they can gather Azolla for free from these river systems or purchase it from other farmers at a significantly lower price than synthetic fertilizers (Carrapiço et al., 2000).</p>
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       <h1 class="title-bg">Picture Based Lesson to Train Farmers</h1>
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[[Image:5.28.jpg|thumb|centre|Picture Based Lesson to Train Farmer|Click on the image to access a higher resolution image as well as lessons adapted for different geographic regions.]]</p> 
<p><i>For the South Asian version (pictures only, text for you to insert), click this link for lesson 5.28:http://www.sakbooks.com/uploads/8/1/5/7/81574912/5.28_south_asian.pdf</i></p>
<p><i>For the East/South Asian version (pictures only, text for you to insert), click this link for lesson 5.28:http://www.sakbooks.com/uploads/8/1/5/7/81574912/5.28e.s.a.pdpdf</i></p>
<p><i>For the Sub-Saharan Africa/Caribbean version (pictures only, text for you to insert), click this link for lesson 5.28:http://www.sakbooks.com/uploads/8/1/5/7/81574912/5.28subsaharan_africa_carribean.pdf</i></p>
<p><i>For the Latin-America version (pictures only, text for you to insert), click this link for lesson 5.28:http://www.sakbooks.com/uploads/8/1/5/7/81574912/5.28latin_america.pdf</i></p>
<p><i>Source: MN Raizada and LJ Smith (2016) A Picture Book of Best Practices for Subsistence Farmers:  eBook, University of Guelph Sustainable Agriculture Kit (SAK) Project, June 2016, Guelph, Canada. Available online at: www.SAKBooks.com</i></p>  
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       <h3 class="title-bg">Additional readings and helpful links</h3>
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          <p>https://www.scientificamerican.com/article/can-the-fern-that-cooled-the-planet-do-it-again/</p>

	<p>Link to an interesting article about how Azolla helps regulate the earth's climate.

http://www.sciencedirect.com/science/article/pii/S0094576508000519</p>

	<p>This article discusses how Azolla my be incorporated into the human diet of astronauts headed 	to Mars.

http://theazollafoundation.org/features/space-and-planetary-colonization/</p>

	<p>This link explains the dietary potential for Azolla in space as well as its ability to purify urine. 	The link also discusses the findings of a Chinese team which demonstrated how 16 m² of 	Azolla can produce enough oxygen for two adults in a controlled ecological life support 	system. 

http://theazollafoundation.org/azollas-uses/other-uses-2/</p>

	<p>Check out this link for more information on some additional benefits of Azolla.

http://www.azollaamrit.com/</p>	

<p>This is a link to an Indian NGO which aims to spread the benefits of Azolla amongst farmers in 	the region.
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       <h3 class="title-bg">References</h3>
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          <p>1.	Azolla Foundation. (2016). Retrieved from
	 	http://theazollafoundation.org/azolla/</p>

<p>2.	Azolla Philippines. (2013). Retrieved from 
		http://www.azollaphilippines.com/how-to-grow--1.html</p>

<p>3.	Bhuvaneshwan, K., & Singh, P. K. (2015). Response of nitrogen-fixing water fern Azolla biofertilization to rice crop. 3 Biotech, 5(4), 523-529.</p>

<p>4.	Carrapiço, F., Teixeira, G., & Diniz, M. A. (2000). Azolla as a Biofertiliser in Africa. A Challenge for the Future. Journal of Agricultural Sciences, 23(3-4), 120-138.</p>

<p>5.	Foster, A.D, & Rosenzweig, M. R. (1996). Comparative Advantage, Information and the Allocation of 	Workers to Tasks: Evidence from an Agricultural Labour Market. Review of Economic Studies, 	63(3), 347-374.</p>

<p>6.	Hasan, M., R., & Chakrabarti, R. (2009). Use of algae and aquatic macrophytes as feed in small-scale 	aquaculture. Food and Agricultural Organization, Rome. </p> 

<p>7.	Kollah, B., Patra, A. K., & Mohanty, S. R. (2016). Aquatic microphylla Azolla: a perspective paradigm for 	sustainable agriculture, environment and global climate change. Environmental Science and 	Pollution Research, 23(5), 4358-4369.</p>

<p>8.	Ludwick, A. E. (1998). Phosphorus Mobility in Perspective. Potash & Phosphate Institute and the Potash 	& Phosphate Institute of Canada, Norcross, GA.</p>

<p>9.	Lumptkin, T.A. (1987). Environmental requirements for successful Azolla growth.International 	Rice Research Institute, Los Banos, Phillippines.  Moody, K., & Janiya, J. D. (1992). Role of azolla in weed control in rice. Philippine Journal of Weed Science, 19, 79-102.</p>

<p>10.	Plants in Stock. (2015). Retrieved from http://www.plantsinstock.co.za/plant_facts_4599_azolla-pinnata</p>

<p>11.	Raizada, M. N., & Smith, L. (2016). A Picture Book of Best Practices for Subsistence Farmers: South Asia 	Version. Guelph: University of Guelph.</p> 

<p>12.	Talley, S. N., Talley, B. J., & Rains, D. W. (1977). Nitrogen Fixation by Azolla in Rice Fields. Basic Life Sciences, 9(1), 259-281.</p>

<p>13.	Talpur, M. A.,  Changying, J.,  Junejo, S. A., Tagar, A. A., & Ram, B. K. (2013). Effect of different water 	depths on growth and yield of rice crop. African Journal of Agricultural Research, 8(37), 4654-	4659.</p>

<p>14.	Vaishampayan, A., & Sinha, R. P., Hader, D. P., Dey, T., Gupta, A. K., Bhan, U., & Rao, A. L. (2001). 	Cyanobacterial Biofertilizers in Rice Agriculture. The Botanical Review, 67(4), 453-516.</p>

<p>15.	Wagner, G., M. (1997). Azolla: A Review of Its Biology and Utilization. The Botanical Review, 63(1), 1-26.</p>

<p>16.	Watanabe, I. (1987). Summary report of the Azolla program of the International Network on Soil Fertility and Fertilizer Evaluation for Rice. Food and Agricultural Organization, Rome.</p> 

<p>17.	Watanabe, I., & Liu, C. (1992). Improving nitrogen-fixing systems and integrating them into 	sustainable rice farming. Plant and Soil, 141(1-2), 57-67</p>
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