Nothing Special   »   [go: up one dir, main page]

Revisión Bibliometrica Azolla PDF

Download as pdf or txt
Download as pdf or txt
You are on page 1of 21

Industrial Crops & Products 183 (2022) 114942

Contents lists available at ScienceDirect

Industrial Crops & Products


journal homepage: www.elsevier.com/locate/indcrop

Review

A state-of-the-art review on the environmental benefits and prospects of


Azolla in biofuel, bioremediation and biofertilizer applications
S. Prabakaran a, T. Mohanraj a, *, A. Arumugam b, *, S. Sudalai c
a
School of Mechanical Engineering, SASTRA Deemed to be University, Thanjavur, India
b
Bioprocess Intensification Laboratory, Centre for Bioenergy, School of Chemical & Biotechnology, SASTRA Deemed to be University, Thanjavur 613401, India
c
Centre for Pollution Control and Environmental Engineering, School of Engineering and Technology, Pondicherry University, Kalapet, Puducherry 605014, India

A R T I C L E I N F O A B S T R A C T

Keywords: This review paper reports the detailed assessment of biofuel (bio-oil and biodiesel) production capabilities and
Azolla filiculoides the potential utilization of Azolla macroalgae in bioremediation and biofertilizer applications. Biodiesel and its
Azolla pinnata blends were utilized in the transportation sector to minimize fossil fuel emissions and greenhouse gas (GHG).
Biodiesel
Another significant biofuel is bio-oil, which is produced by pyrolysis of biomasses. High energy density combined
Bio-oil
with easiness of storage and transportation of bio-oil compared to gaseous products, bio-oil is considered a
Bioremediation
Biofertilizer possible source to replace petroleum fuel for power production. The key reason for choosing Azolla species as
feedstock for biofuel production is its sustainability, high lipid and energy content. Besides, the Azolla grows in
simple wetlands and wastewater, which is efficient and cost-effective. The results from the various literature
ensured that the Azolla based biofuels are a better alternative to fossil fuels. The wastewater from the industries
and nuclear power plants contains pollutants such as heavy metals and metalloids. Heavy metals cause several
damage to the ecosystem. The conventional methods of treating wastewater are expensive and time-consuming,
whereas the bioremediation method provides low-cost alternate methods. The removal of heavy metals from
wastewater is achieved using Azolla algae, a biological source present in ditches and ponds. Azolla quickly
spreads as a dense layer over the water surface and adsorbed heavy metals from the wastewater. The current
study critically reviewed the Azolla’s potential capacity to be used in the phytoremediation method and remove
the heavy metals from wastewater to better environmental conditions. In addition, Azolla is reported as a bio-
fertilizer and green manure in gardens and rice fields due to their high cellulosic content.

increase in CO2 emissions due to rising energy demands over previous


decades. According to Fig. 1, the projection of global energy consump­
1. Introduction tion for each year results in the world energy demand will increase
(Perera, 2018). Transitioning away from traditional fossil fuels and to­
Since the beginning of industrialization, fossil fuels have been the wards cleaner energy, renewable energy sources is the potential strategy
backbone of the industrialized world’s economic development (Bhuyar for reducing GHG emissions, stabilizing the global climate and
et al., 2020; Islam and Hasanuzzaman, 2020; Jayakumar et al., 2021). improving energy security (Dahlke et al., 2021; David et al., 2021).
Currently, fossil fuels account for nearly 80% of global energy produc­ Biofuels, solar, hydro, geothermal and wind are the primary renewable
tion, including oil (33%), natural gas (27%), and coal (20%). However, sources that may produce energy while emitting fewer GHG and atmo­
the world’s reliance on fossil fuels creates a critical issue of emissions spheric pollutants (Rafiee and Khalilpour, 2018). Biofuels are un­
(Nurul Aina Nasriqah Binti et al., 2021; Paramasivam et al., 2021). In doubtedly a promising renewable source in the transport sector
many areas, industrialization and urbanization are the primary sources compared to remaining renewable sources. All other renewable sources
of pollution. Furthermore, energy generation from fossil fuels is the can provide electricity and thus cannot compete with oil on an equal
primary source of greenhouse gas and CO2 emissions (Bhuyar et al., footing (Abusweireh et al., 2022; Arutyunov and Lisichkin, 2017).
2021; Mahmood et al., 2020). The consumption of fossil fuels is inex­ Furthermore, biofuels could be used with existing facilities and
tricably linked to global warming and extreme weather events caused by needless technical improvements than other energy sources. As a result,
industrial emissions (Ahmad et al., 2021). Fig. 1 shows the significant

* Corresponding authors.
E-mail addresses: aruchemxl@scbt.sastra.edu (T. Mohanraj), aruchemxl@scbt.sastra.edu (A. Arumugam).

https://doi.org/10.1016/j.indcrop.2022.114942
Received 1 March 2022; Received in revised form 8 April 2022; Accepted 10 April 2022
Available online 19 April 2022
0926-6690/© 2022 Elsevier B.V. All rights reserved.
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Nomenclature FN Farmers Nitrogen


FNA Farmers Nitrogen combined with Azolla biofertilizer
BHU Banaras Hindu University FTIR Fourier Transform Infrared Spectroscopy
BNF Biological Nitrogen Fixation GCMS Gas Chromatography-Mass Spectrometry
BSEC Brake Specific Energy Consumption GHG Greenhouse Gas
BSFC Brake Specific Fuel Consumption HBP Histamine Binding Protein
BTDC Before Top Dead Center HC Hydrocarbon
BTE Brake Thermal Efficiency HPLC High-Pressure Liquid Chromatography
B20 20% of Biodiesel Blend IC Internal Combustion
B30 30% of Biodiesel Blend IRRI International Rice Research Institute
CO Carbon monoxide NOx Oxides of Nitrogen
COD Chemical Oxygen Demand. NPK Nitrogen, Phosphorus and Potassium
CO2 Carbon dioxide RN Reducing farmer’s Nitrogen
CI Compression Ignition SEM Scanning Electron Microscopy
CRRI Central Rice Research Institute SMU Sebelas Maret University
DAB Deoiled Azolla pinnata Biomass SNRC Spanish National Research Council
DU Diponegoro University SOC Soil Organic Carbon
EDX Energy Dispersive X-Ray Analysis TAA Tetraalkylammonium Salts
EPA Eicosapentaenoic Acid UAE Ultrasound-Assisted Extraction
FA Fatty Acid USA United States of America
FAME Fatty Acid Methyl Esters WoS Web of Science
FESEM Field Emission Scanning Electron Microscopy WW Waste Water
FFA Free Fatty Acid XRD X-Ray Diffraction
FID Flame Ionization Detector

industrialized and emerging nations have concentrated on increasing Astolfi et al., 2020). Second-generation biofuels are derived from agri­
their biofuel markets and establishing intergovernmental policies for culture residues or cellulosic matters, including leaves, grass and woods
biofuel usage (Malmgren and Riley, 2018). The implementation of such (Jutakridsada et al., 2019). Third generation biofuels are generated
rules, notably in Brazil, the United States and Europe, has resulted in the using cultured aquatic feedstock, such as algae. Algae were revealed to
growth of biofuel production over the last 20 years, with biofuels offer tremendous capability as feedstocks to provide substantially
currently accounting for roughly 3% of all transportation fuel consumed greater yield with lower resources. Additional environmental benefits of
globally (Khan et al., 2021). Biofuels are classified into four groups using algae include its capacity to fix CO2, which was suggested to
depending on the feedstock required for manufacturing and technical remove CO2 from power plant flue gases, hence lowering GHG emissions
advancement in the production process. First-generation biofuels are (Choi et al., 2019; Kumar et al., 2018). Genetically altered microor­
made from edible sources like maize, oilseeds (palm, soybean, rapeseed) ganisms produce fourth-generation biofuels, such as bioengineered
and sugar cane (Dahman et al., 2019; Rajeswari et al., 2022). Fig. 2 algae, fungus, cyanobacteria, and yeast. Other than first-generation
represents that in the past decade, palm oil provides such biggest share feedstocks, the remaining feedstocks are considered advanced biofuels
of feedstock next to soybean and rapeseed oil. Biofuel provides only a sources and are expected to offer several benefits; nevertheless they are
marginal improvement as GHG reduction over fossil fuels since it con­ still in the research stage and have not achieved their complete market
sumes a considerable amount of energy to cultivate and harvest (Luiza potential (Shin et al., 2016). Azolla does not belong to oilseed feedstock,

Fig. 1. Trends of global energy consumption, CO2 emission, biofuel production, and renewable energy consumption in the past two decades.

2
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

A large proportion of wastewater is released from textile, distillery,


tanning and domestic wastes. Issues become more complex when the
quantity of wastewaters increases (Adane et al., 2021; Islam, 2020).
Heavy metals are the contaminations of industrial waste such as mill
tailing, nuclear waste disposal etc (Mohammadi et al., 2021). These
heavy metals are highly toxic and non-biodegradable due to their
high-water solubility and have a long half-life in the environment. For
the benefits of environmental remediation, the removal of heavy metals
from wastewater is increasing (Ali et al., 2019). To avoid contamina­
tions in surface water, the metals in wastewater must be carefully
treated using wastewater treatment plants. The conventional treatment
systems involve biological and physicochemical unit processes. This
system costs heavily in treating the wastewater because of human re­
sources and labor skills (Oladoja, 2017). Natural treatment systems are
ecologically engineered wetlands and considered more sustainable for
wastewater treatment. Phytoremediation is a method to eliminate toxins
from the environment by utilizing green plants. Much attention has been
Fig. 2. Percentage of various feedstocks used for biodiesel. turned to phytoremediation because using plants to treat polluted en­
vironments is a significant alternative source (Ansari et al., 2020; Babu
et al., 2021; Mahajan and Kaushal, 2018; Yan et al., 2020). The rela­
reducing the crushing and processing costs. Azolla can be cultivated in
tively new technology for biosorption uses aquatic plants to solve the
confined pools at a minimum price shown in Fig. 3. Even though its oil
problems of heavy metals. The preference of plants depends on good
yield is not higher than certain microalgae, adopting these macroalgae
morphological properties, availability, non-hazardous nature,
for biodiesel production offers some advantages over the ecological
cost-effectiveness, and efficiency (Al-Baldawi et al., 2018; Gholizadeh
difficulties created by microalgae (Chisti, 2007). This review focussed
et al., 2020; Talebi et al., 2019). This review focuses on using a natural
on Azolla as the feedstock for biofuel production. Azolla is the most
organism known as Azolla.
sustainable, attractive feedstock for its low maintenance, lower-cost etc.
Azolla is considered in the family of Salviniaceae. Azolla, blue-green
It is used in a broad spectrum of renewable fuels. The amount of oil
algae and a small free-floating plant are commonly found in ditches
extraction from Azolla against other feedstock is acceptable as biodiesel.
and ponds. It grows in partial treated domestic wastewater (WW)
Fig. 3(d) shows the extracted Azolla bio-oil from the biomass and
(Banach et al., 2020; Jones et al., 2016). The growth rate increases with
transesterified Azolla biodiesel. In addition, creating biomass from
increasing photoperiod, at temperatures up to 30 ◦ C, and the optimum
Azolla is often not a great expense than cultivating the crop (Mandal and
pH value is 6.5–7.5. The colonizing form grows most rapidly, doubling
Mallick, 2011).
times as few as five days and absorbing heavy metals from the waste­
The major issue is the pollution produced by poorly treated and
water (Sood et al., 2012). Biomass of Azolla contains unique chemical
untreated industrial wastewaters (Briffa et al., 2020; Ilyas et al., 2019).
composition and accumulates on each leaf, such as lignin,

Fig. 3. (a), (b) & (c) Azolla Pond cultivation (d) Azolla oil & Azolla biodiesel.

3
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

carbohydrates, and inorganic matter. The growth of Azolla in WW im­ biofertilizer for pollution-free agriculture and to improve soil produc­
proves the quality of discharged water by controlling the eutrophication tivity was extensively reported.
of natural water (Yadav et al., 2016). Specifically, when Azolla grows in
domestic wastewater, the phosphorus content is five times higher than 2. Azolla: International market and development
in natural waters (Sadeghi et al., 2013). The removal of heavy metals
using chemicals generates high sludge, whereas using biosorption Azolla is the genus of aquatic ferns characterized by a small free float
methods, removing heavy metals by aquatic fern reduces the concen­ sporophyte composed of closely packed stems (De Benedetti et al.,
tration to very low levels (Temmink et al., 2018). 2018). Azolla has been used to fix the ambient nitrogen through sym­
Azolla is a small free-floating aquatic fern that grows well in partially biotic relations with blue-green algae. Azolla fern is indigenous to Asia,
treated domestic wastewater. Azolla lives in a symbiotic relationship America and African countries; these species naturally thrive in wet­
with the nitrogen-fixing cyanobacteria. The main advantage is distri­ lands, streams, wastewaters, as well as other water bodies (Hashemloian
bution in various wastewaters and colonizes rapidly as a mass dense and Azimi, 2009). A few species have spread over different regions of the
covering over the water surface (Miranda et al., 2020). It has a high earth through artificial, or natural sources were shown in Fig. 5
amount of biomass yield, adsorption and concentration ability of met­ (Lumpkin and Plucknett, 1981). This is a versatile crop that could use as
alloids and heavy metals from the aqueous solution, which has high poultry and fish feed, biofertilizer and decontamination reagent. Azolla
potential use in phytoremediation. Azolla can be utilized as a biofilter to has been discovered to be an effective biofertilizer and food for fish in
purify wastewater and feedstock for terrestrial and aquatic animals due Bangladesh. It was considered a subtropical crop, and the Chinese
to its mineral, proteins and fiber content (Miranda et al., 2018). proved successful in developing it directly in paddy fields before
Modern agricultural systems encounter plenty of difficulties that transplanting (Bocchi and Malgioglio, 2010). In the late nineteenth
threaten food security and nutrition. Chemical pesticides and fertilizers century, Azolla was just being farmed in prime location throughout the
are used on a wide scale to improve agricultural output to meet the east Asian shoreline far as south approximately 200 N latitude near
nutritional needs of the global population. However, excessive use of Vietnam’s red river delta and then northeast via Fujian regions to the
chemical pesticides has caused environmental pollution, creating health vicinity of Wenzhou area Zhejiang region China near 280 N latitude
risks(Mahmud and Chong, 2021; Raimi et al., 2021). Furthermore, (Brouwer et al., 2018).
agricultural soils are losing its physical properties along with biological At the start of 1960, a significant effort to extend the usage of Azolla
and overall chemical (nutrient imbalance) health. Chemical fertilizers started in China and Vietnam. Following the revolution in Vietnam and
containing (N, P, or K) are used too much in modern agricultural systems China, the newly elected government recognized the benefits of Azolla
to meet plant nutritional requirements and increase crop yields (Kumar and started authoritatively promoting its application and developing the
et al., 2022). Owing to low fertilizer usage efficiency, only a small propagation hubs (Mohamed and Abd-elsalam, 2021). Throughout the
portion (30 – 40%) of such nutrients are taken up by the plants, with the colonial period in Vietnam, French researchers revealed the usage of
balance becoming lost to the soil, producing pollutants (Chittora et al., Azolla and conducted the initial investigation of its farming. Therefore,
2020). The use of microphytes and macrophytes as biofertilizers in at the end of the colonial era, Azolla was planted on approximately 40,
sustainable agricultural methods has developed as a revolutionary and 000 ha as a winter green manure for springtime rice cultivation. To
environmentally acceptable method of enhancing soil fertility and plant encourage utilization, the new government developed an Azolla research
growth. Many microbes in the microphytes perform critical roles in the laboratory at the crop cultivation research institute in 1958, as well as
progression of agriculturally essential crop plants (Kour et al., 2020). an extended system including over 1000 inoculum production sites
Biofertilizers are live or dormant cells added to soil and seed to improve (Lumpkin and Plucknett, 1981; York and Garden, 2016). Vietnam re­
plant nutrition and absorption from the soil. Biofertilizers have devel­ searchers have gathered approximately 30 types of indigenous Azolla,
oped as a more cost-effective and ecologically responsible substitute for and better strains for warmth, salt, cold and acid resistance have been
chemical-based fertilizers (Pradhan et al., 2022). Substantial improve­ developed. In China, Azolla based research activities were risen
ments have actually been made in the creation of efficient biofertilizers dramatically, as have outreach efforts to encourage its usage. Azolla has
for several crops. The analysis of Azolla biomass shows great potassium, become farmed as green manure for approximately 1.3 million hectares
phosphorus, nitrogen, and organic matters favor the usage of bio­ of paddy across China (FAO, 1978). Several rice research institutions in
fertilizer in paddy fields (Abd El-Aal, 2022). Fig. 4. Shows the classifi­ underdeveloped countries have yet initiated Azolla research with suc­
cation of Azolla biorefinery. cessful results. The most effective initiative is likely to be in Thailand.
This review work aims to provide an in-depth examination of the The Ministry of Agricultural department has financed an Azolla initiative
usage of Azolla species in bio-oil, biodiesel, bioremediation, and bio­ program that proceeded via provincial development centers and now as
fertilizer applications. Azolla has a high biofuel content, used to operate the level of commercial farms on farmers’ fields (Das et al., 2018). In the
the unmodified CI engine to reduce emission parameters. This review United States, three prominent Azolla research centers were developed.
critically describes Azolla as a promising biofuel production feedstock. At the University of Hawaii, agricultural and physiological research is
The prospect of Azolla as non-toxic natural wastewater (WW) treatment conducted to describe and determine the use of these Azolla in tropical
reagent and their environmental benefits were thoroughly discussed. In farming systems. The research goal at the University of California, Davis,
addition, the potential ability of Azolla as an environment-friendly is on Azolla cultivation in subtropical regions. The work at the Kettering

Fig. 4. Classification of Azolla biorefinery.

4
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Fig. 5. The global distribution of Azolla species.

laboratory focuses on common physiological investigations to better the scholarly documents. The US is on the top list of both commercial
understand the Azolla to Anabaena interaction (Kollah et al., 2016; and scholarly document publications. China has less public than com­
Peterson et al., 2020). In the United States, it is quite likely that less than mercial documents. These data articulate the potential for commer­
$300,000 each year is presently being spent on Azolla research. India, cialization of Azolla in countries like India, Indonesia, the UK, Iran,
Thailand, Nepal, Burma, Bangladesh, Malaysia, Indonesia, Sri Lanka, Australia and the Netherlands. Figs. 6 and 7 represents the non-
Peru, Egypt, and The Philippines is among the countries that started commercial and commercial document from a different jurisdiction.
Azolla research presently. Furthermore, numerous additional countries
have expressed interest in ferns and their applications (Watanabe et al.,
3.2. Trends of the publications
1992).

The maximum number of research and commercial articles was


3. Scientometric assessment
published between 2010 and 2020. The details of research publications
record a totally of 5138 articles from the year 1950–2020, among which
The significant growth of the publishing sector has mandated the
1808 documents were published during the year 2015–2020. Regarding
assessment of scholarly publications. Many tools were developed to
the patent, 619 articles were recorded between 1950 and 2020, among
assess the knowledge products for the mining of rightful information
which 58 articles were documented during the period of 1950–2000,
(Konur, 2020; Saravanan et al., 2022). The outcome of this assessment
and 130 documents were recorded during 2015–2020. A maximum of 63
may help us understand the evolution of scientific studies and summa­
patents were filed in 2016, and 40 patents were granted during the year
rize various useful information, including the trend, productivity, and
2020. This trend is evident that research and commercialization of
impact of the research publications (Qiu et al., 2021; Zhang et al., 2022).
Azolla are picking its potential in recent years, and the growth is grad­
The process of Scientometric can also help us identify the research
ually increasing. Fig. 8 represents the trends in public scholarly
group, institution, research priorities, standards, strengths, and weak­
documents.
nesses of any aspect of the research subjects (Andreo-Martínez et al.,
2020; Sabe et al., 2022). The present Scientometric study is limited to
3.3. Institution and researchers
the trends, researchers, and countries actively involved in Azolla
research. The public scholarly documents like journal articles, books
The institution involved in the publication of public scholarly
chapter, dissertations, and commercial scholarly documents like patents
document between the year 1950–2020 has mentioned in Fig. 9 and
were squared up at a single platform, namely LENS.org. The open
Fig. 11, and the recent years 2015–2020 is mentioned in Fig. 10. The
database LENS.org is featured to connect and compare the patent and
International rice research institute (IRRI), Central rice research Insti­
non-commercial databases, gaining interest from policymakers, scien­
tute (CRRI), and Banaras Hindu University (BHU) were leading con­
tists, and investors. The database centered on Azolla from LENS.org was
tributors during 1950–2020. During the year 2015–2020, the
tracked and analyzed. The scholarly work accounts for 5138 documents,
Diponegoro University(DU), Sebelas Maret University(SMU) and Span­
and 619 patents were recorded.
ish National Research Council(SNRC) are topping. This may be due to
the absence of a research group involved in the active research of Azolla
3.1. Countries actively involved during the early years. The leading institution IRRI has brought 47 ar­
ticles, and the maximum record was documented during 1983–1993;
India leads the scholarly document publications, followed by the US CRRI registered a totally of 38 documents, and their peak publications
for the assessment period 1950–2020; from 2015 to 20, Indonesia leads were during the year 1988. BHU consistently contributed to the

5
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Fig. 6. Document counts of Scholarly work.

Fig. 7. Document counts of patent.

publications and recorded 31 articles from 1989 to 2020. DU from publications were published in the year 2020–2002. 23.67% of articles
Indonesia is the leading contributor during the year 2015–2020, and were published in Environmental Science and 5.75% in Environmental
they started the research in 2014 and contributed 19 documents during engineering based on the web of science category. Whereas in the Sco­
2019 maximum of 6 articles has been published. Regarding the contri­ pus database, the environmental documents share 16.8% of articles and
bution of Azolla, P.K Singh, S.Kannaiyan and I.Watanabe, contributed Agriculture and biological Science account for 36.5% of documents. The
more articles for the entire assessment period of 1950–2020. for the citation report from WOS summarizes 9710 citing articles and among
period of 2000–2020, Davoud Balarak, Ana Luisa Pereira, are the top which 9085 articles are without self-citation, and H- Index is 5.
two contributors; from 2015 to 2020, Henritte Schluepmann, from The
Azolla HS Lab, Utrecht University, Arnab Kumar De, from University 3.5. Bibliographic assessment
Kalyani lead the publication.
The bibliographic Assessment was conducted using the Scopus
3.4. Summary of information analysis from Scopus and WoS database for co-authorship, VOS viewer tool was used for the analysis.
The VOS Viewer tools identified 3949 authors from the 1712 articles;
The Scopus database accounts for 1712 documents from 1882 to the analysis was framed based on the author’s contributions using the
2022, with a maximum publication of 129 documents in the year 2021. full counting method. For each of the 131 authors, the tool calculated
The web of Science database has 887 collections, and a maximum of 94 the total strength of co-authorship links with other authors. Forty-one

6
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Fig. 8. Trends of Public documents.

Fig. 9. Documents published by the institution during 1950–2020.

clusters were identified by the tool by recognizing the largest connected et al., 2017; Whangchai et al., 2021). Utilization of biodiesel results in
item with greater link strength. Fig. 12 represent the density visualiza­ zero net increase of CO2 and significantly less amount of sulfur contents.
tion on co-authorship based on link strength. Among 41 clusters, four Biodiesel has essential economic potential because of its non-renewable
clusters have more than ten items. The overlay visualization of the same fuel, which has fossil fuel prices that will increase further (Hoang, 2021;
results explicit the time scale and of the clusters. Fig. 13 denotes the Jayakumar et al., 2021). Only a few amounts of literature have been
clusters with the authors Singh, P.K and Watanabe, I, Tel-or, and Gun­ published to the depth of our knowledge on the biotransformation of
ning, who contributed before 2010 (1990–2010). The clusters with au­ Azolla to a useful product. The classification of catalysts used for the
thors Cheng and Brouwer, Recihart, and G-J were represented after 2010 biodiesel production process is shown in Fig. 14.
(2010–2020). Miranda et al. (2020) analyzed the reproductive and vegetative
stages of Azolla to yield lipids in response to stress. In a male, micro­
4. Biodiesel spores and microsporocarps have high lipid droplets containing tri­
acylglycerol. Redirection of fatty acid to anthocyanin by carbon flow
After the bioremediation process, the treated Azolla biomass can be pathways changes the yield & composition of fatty acid. The degree of
transferred to many useful products (Naghipour et al., 2018). The most unsaturated fatty acids (FA) and the length of lipids satisfy the impor­
promising way of bio transforming the Azolla is biodiesel. Biodiesel is tance of biodiesel standards. Azolla filiculoides show a high total yield of
produced from the algal biomass oil and most common vegetable oils. lipids and productivity rate at the reproductive stage, which suits biofuel
The main reason for focusing on biodiesel is because it can be sustain­ production. Golzary et al. (2021) this study show the enhancement of
ably supplied and has several favorable environmental properties (Khan the growth rate of Azolla and the extraction of lipids for the production

7
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Fig. 10. Document published by the institution during 2015–2020.

Fig. 11. Authors contributed for Scholarly publication from 1950–2020.

of biodiesel. At 22 ◦ C, it offers a high growth rate and light intensity of detected, and tannic acid pretreatment was effective for enhanced bio­
20 lx, 75% humidity, 6.4 pH for 2.1 days, and lipid content of 11.7%. As methane production. The maximum yield of 250.1 ml/gVS where the
a result, Azolla can be used as feedstock for biorefineries and wetlands raw biomass was 12% lesser than tannic acid-free. (Pirbazari et al.,
conservations. 2019) study the effects of Azolla filiculoides by the pyrolysis method. The
Dohaei et al. (2020) about the integrated biorefineries for bioenergy Non-catalytic pyrolysis was conducted at 400–700 ◦ C, in which the
and biochemical production using Azolla filiculoides. The raw biomass maximum yield of bio-oil was at 500 ◦ C. At an optimum temperature of
contains lignin 12%, carbohydrates 41.4%, and inorganic matter 10.3%. 500 ◦ C, the chemical composition of bio-oil and a high amount of syn­
To enhance the nutritional values and estimate the yield of proteins, thesis gas were obtained when conducted in the dual bed quartz reactor.
phenolic compounds and lipids were extracted. Residues after the Mg-Ni-Mo/MPC, pyro char and modified pyro char are the three best
extraction are used for biogas production. Lipid yield from biomass was catalysts used in common reactions, in which the furan compound
rich in Eicosapentaenoic acid (EPA) and palmitic acid at 18.1%. The two increased (5.25–33.07%) and decreased (25.56% and 9.09%) by the
protein extraction methods are ultrasound-assisted water by NaOH & incredible result of Mg-Ni-Mo/MPC. The carbon-based catalysts ana­
sequential extractions of hot trichloroacetic acid. Ultrasound-assisted lysed by EDX, FESEM and gases and liquid products were analysed by
extraction (UAE) extracted 24.4% protein and 11.9% of the GC FID and GC MS. Salehzadeh et al. (2014) work on the potential of
water-soluble protein at optimum conditions. The fern protein contains Azolla filiculoides for biodiesel production. Azolla filiculoides were
37.9% of tetraalkylammonium salts (TAA); the most abundant is glu­ collected from the rice farm in northern Iran. The Azolla was
tamic acid, 20.5%. In high-pressure liquid chromatography (HPLC) freeze-dried, and Solvent was extracted using Soxhlet apparatus, which
analysis, luteolin, chlorogenic acid, tannic acid & caffeic acid were contains methanol-chloroform (1:2 v/v) to produce crude oil. The

8
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Fig. 12. Density visualization of co-author weighed based on the document.

Fig. 13. Overlay visualization of co-author weighed based on document and scored on publication per year.

acid-catalyzed methylation technique used the acid-catalyzed trans­ productivity, which produces at 800 ppm and utilizes the CO2 from the
esterification to produce a fatty acid, monoglycerides, triglycerides, & industry. The DW of crude lipids from harvested biomass contains 7.92
diglycerides to FAME. In macro algae biodiesel, GC–MS was used to ± 0.14%. The Drying conditions were energetically optimized and did
analyse the FAME. The presence of various acids in the macroalgae not affect the lipids. Extraction of total lipids 4.2 ± 0.38% (FFAs). The
shows biodiesel was confirmed. As a result, Azolla can be used as a FAs (41 ± 13%) converted to FA methyl esters in methanol by saponi­
source for biodiesel production due to its low cost and availability. fication process. Nearly 7.2 ± 2.8% of di-hydroxy compounds constitute
Brouwer et al. (2016) analyse the lipid fraction of Azolla filiculoides crude lipids. These hydroxy compounds were removed by fractionation
for biodiesel production. At high concentrations of CO2, Azolla has high step, which increases biodiesel quality from the Azolla filiculoides lipids.

9
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Fig. 14. Classification of catalysts used for biodiesel production.

The secondary product stream provides di-hydroxy FAs and long-chain wastewater. Mechanical and chemical extraction techniques were
alcohols, which apply to the nutrition and chemical industries. Table 1 adopted to extract the lipids from the microalgae, and the trans­
shows the usage of Azolla in the biotransformation process. esterification process was used to produce biodiesel (Jacob et al., 2021).
Prabakaran et al. (2021) Produced the Azolla pinnata biodiesel yield
5. Performance and emission analysis (88.7%) for optimized process parameters of methanol-Azolla oil molar
ratio (30:1), operation temperature (70 ◦ C) and catalyst weight (4%)
The concept of utilizing biofuels in conventional diesel engines arose using the heterogeneous catalyst. When Azolla pinnata biodiesel was
when its inventor, Rudolf Diesel, unveiled peanut oil as a substitute in used in a single cylinder CI engine, the biodiesel blend (B30) reduced the
the first diesel engine at the Paris world fair in 1900. Biofuels are engine emissions such as HC (12.06%), CO (14.0%), smoke (5.88%) and
essential due to their renewable nature, whereas fossil fuels are limited a slight increase in NOx (2.46%) related to diesel fuel. Subsequently, the
(Ogunkunle and Ahmed, 2019). Regardless of weather conditions, bio­ drop in BTE (10.2%) and the rise in BSFC (17.3%) were observed. Pra­
fuels can operate many diesel engine vehicles. Furthermore, Enhancing bakaran et al. (2021) Alumina nanoparticles (50 ppm) dosed Azolla
the development of liquid biofuels, like biodiesel, could increase the pinnata blends (B30) in IC engine were resulted in a decrement of HC
accessibility of a cleaner, less expensive source compared to fossil fuels (24.4.%), CO (21.24%) and smoke (15.25%) compared to diesel due to
(Karpanai Selvan et al., 2022; Soudagar et al., 2018). In recent years, their improved cetane number and calorific value. The inclusion of
various bio-lipids have been utilized to produce biofuels. Microalgae has Alumina nanoparticles influenced the performance parameters of the CI
the ability to produce a variety of sustainable biofuels, including bio­ engine by increasing BTE (8.41%) and reducing BSEC (6.37%)
diesel, bioethanol and bio-hydrogen (Alam et al., 2015). Microalgae compared to the B30 blend. The effects of incorporating Bao, Bi2O3 nano
production does not necessitate the use of chemicals such as herbicides additives at different concentrations (25 ppm, 50 ppm, 75 ppm and
and pesticides. Subsequently, it can be cultivated in saltwater as well as 100 ppm) with B20 Azolla biodiesel blend were investigated in the diesel

Table 1
Azolla in biotransformation process.
Product Process parameters Temperature Time duration Yield Reference

Lipid extraction Humidity 75%, Light intensity 20 lx, 22 ◦ C 2.1 days Lipid content extraction from Azolla is (Golzary et al., 2021)
pH 6.4 11.7%.
Biodiesel production Methanol to oil ratio (6:1) and 10 ml 60 ◦ C 45 min The maximum yield of around 8.25 g is (Subramaniam et al.,
of H2SO4 obtained 2020)
Extraction of phenolic, Biomass kept in anaerobic conditions 37 ℃ 7–10 days Maximum lipid yield of 18.1%; Phenolic (Dohaei et al., 2020)
protein, lipid & contents of 27.2 mg gallic acid, 24.4% of
methane production. protein and methane yield 250.1 ml/gVS.
Bio-oil production Catalytic pyrolysis proceeded in a 500 ◦ C 2h Bio-oil yield is 35 wt%. (Pirbazari et al., 2019)
dual-bed quartz reactor
Lipid production Ground plant materials (25 mg) were 23–26 ◦ C Total run time Crude lipids from A. filiculoides can be (Miranda et al., 2018)
extracted in 4 ml of chloroform/ 42 min; solvent estimated as 1.68 t/ha-year
methanol (2:1, v-v) delay 4.1 min
Biofuel production – – Treatment period 5 Ethanol production from Azolla filiculoides (Miranda et al., 2016)
days is 11.7 × 103 L/ha year.
Biooil and biodiesel 5 ml of extracted lipid fraction mixed – Refluxed period 4 h Oil yield in Azolla filiculoides was 15% by (Salehzadeh et al.,
Production with 75 ml of 2% H2SO4 weight of dry biomass. 2014)
Lipid extraction Ground Azolla biomass was Soxhlet- – 24 h 7.92 ± 0.14% dry weight (dw) crude (Brouwer et al., 2016)
extracted with a 7.5:1 lipids
dichloromethane (DCM) to methanol
Biodiesel The methanol-oil molar ratio (20:1), 75 ◦ C 5h Biodiesel yield 90.77% (Prabakaran and
KOH catalyst (3 wt%) and Mohanraj, 2021)
Biodiesel Methanol to oil molar ratio (30:1), 70 ◦ C 8h Biodiesel yield 88.7% (Prabakaran et al.,
Heterogeneous catalyst weight% 2021)
(4 wt%)
Biodiesel Methanol to oil molar ratio (9:1), 1% 90 ◦ C 1h – (Kannan and Christraj,
of sulfuric acid (H2SO4) 2018a, 2018b)
Biodiesel A 110 ml of ester in which eight 55–60 ◦ C 2h – (Narayanasamy and
pellets of KOH catalyst with 52 ml of Jeyakumar, 2019)
methanol
Biodiesel Raw oil to methanol ratio (5:1); 17 g 65 ◦ C 2h – (Thiruvenkatachari
of KOH per liter of raw oil et al., 2021)

10
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

engine, which provides the reducing trend of HC, CO and smoke only enzymes or microbes in the constructed wetlands to remove the pollu­
except for the NOx emission (Prabakaran and Mohanraj, 2021). The tion from the environment (David et al., 2021; Ojuederie and Babalola,
properties of various concentrations of (25 ppm, 50 ppm, 75 ppm and 2017). This technique is cost-effective and environmentally friendly in
100 ppm) TiO2 added Azolla pinnata blend (B20) were measured as per the revitalization of the environment. Bioremediation of heavy metals
ASTM standard. The biodiesel blend dosed with TiO2 (100 ppm) nano has its own limitations. Macrophyte utilization for the treatment of
additive showed better results than the other test fuels. The experi­ wastewater has been reported frequently. A free-floating aquatic
mental analysis reveals the test fuel (B20 + TiO2 100 ppm) lowers the macrophyte like ferns is capable of carrying out bioremediation activ­
HC (12.97%), CO (57.3%), smoke (36.04), BSFC (23.53%) and increases ities (Kochi et al., 2020; Kurniawan et al., 2021).
the BTE (13.38%) and NOx (9.16%) values than B20 blend (Nar­ In the recent decade, there has been a surge in interest and support
ayanasamy and Jeyakumar, 2019). The performance, emission and for phytoremediation. Along with its effectiveness with other traditional
combustion parameters were investigated for Azolla pinnata blend B10, procedures, this environmental sustainability green technology has
B20, B30, B40 and B100 in a diesel engine with injection timing 27◦ received increasing attention. Phytoremediation is a bioremediation
before top dead center (bTDC). B20 results show better performance technique that employs Azolla species to remove, stabilize, transfer and
parameters among fuel blends, and the B30 blend provides excellent eliminate pollutants in wastewater and soils (Yan et al., 2020). Chemical
emission results (Subramaniam et al., 2020). Azolla microphylla algae compounds generated by the Azolla retain the impurities instead of
expand on the water surfaces and may be a possible future feedstock for decomposing them throughout this process. Furthermore, this phytor­
the preparation of biodiesel. The prepared biodiesel was tested in a CI emediation treatment employed for wastewater produce and cause
engine to analyze the performance and emission characteristics. Azolla irreversible changes to the water characteristics. It has been identified as
microphylla biodiesel was derived from the transesterification process, a low-cost, environmentally benign way of removing heavy metals from
and its blends B25, B50, B75 and B100 were tested in a 5.2 kW diesel polluted areas. Phytoextraction is the important mechanism among all
engine with a constant speed of 1500 rpm. The results depict that other phytoremediation processes (phytovolatilization, phytostabiliza­
increasing the blend ratio increases the HC, CO and smoke emission and tion, phytodegradation, phytostimulation and phytofiltration) in which
reduces the BTE and NOx for both part load and full load conditions Azolla remove heavy metals from wastewater shown in Fig. 15. It is the
(Thiruvenkatachari et al., 2021). The impacts of Azolla biodiesel in process by which pollutants from wastewater are taken up through roots
compression ignition engine were listed in Table 2. The properties of translocated and accumulated in the Azolla biomass. Generally, Azolla
different Azolla species are listed in Table 3. can absorb the metals from wastewater. Moreover, it can collect, extract,
and tolerate significant quantities of heavy metals in its structure (Goala
6. Bioremediation et al., 2021). Phytovolatilization is the mechanism through which Azolla
absorbs and transpires contamination, followed by the discharge of the
Heavy metals are the contaminations of industrial waste such as mill contamination or a mutated form of the contaminant into the atmo­
tailing, nuclear waste disposal etc. Accumulation of heavy metals in the sphere. Most pollutants can move via the roots to the leaves and then
environment is highly toxic and non-biodegradable due to its high-water volatilize into the environment at relatively low amounts throughout
solubility and long half-life (Selvi et al., 2019). For the benefits of this process (Tangahu et al., 2011).
environmental remediation, the removal of heavy metals from waste­ Azolla is one of the hyperaccumulator plants which can absorb heavy
water is increasing. To avoid contaminations in surface water, the metals 50–500 times faster than conventional plants; it has significantly
metals in wastewater treatment plants must be carefully treated helped the revolutionary progress of the phytoextraction technique.
(Mohammadi et al., 2021; Rajendran et al., 2022). Analysis of heavy Heavy metals are described chemically as elements having metallic
metal performed under atomic absorption. Bioremediation transforms characteristics, an atomic number greater than 20, and a specific gravity
the highly toxic heavy metal into a less harmful product by using the greater than 5. the most frequent heavy metal pollutants are Cr, Cd, Cu,

Table 2
Utilization of Azolla biodiesel in compression ignition engine.
Engine Testing Reference fuel Test fuel Emission Performance Reference
condition

Kirloskar PS/234, single-cylinder, 4- Constant Diesel 30% Azolla pinnata biodiesel ↓: CO, HC, ↓: BTE (Prabakaran et al.,
Stroke (4 S), Rated Power (RP): speed, variable + 70% Diesel smoke ↑: BSEC 2021)
3.75 kW, 1500 rpm, Compression Ratio load ↑: NOx
(CR) 18:1
Kirloskar PS/234, single cylinder, 4 S, RP: Constant 30% Azolla pinnata 30% Azolla pinnata biodiesel ↓: CO, HC, ↓: BSEC (Prabakaran and
3.75 kW, 1500 rpm, CR 18:1 speed, variable biodiesel + 70% + 70% Diesel + 50 ppm Al2O3 smoke ↑: BTE Mohanraj, 2021)
load Diesel Nanoparticles ↑: NOx
Single cylinder, 4 S, RP: 5.2 kW, Constant 20% Azolla 20% Azolla biodiesel + 80% ↓: HC, CO, – (Kannan and Christraj,
1500 rpm, CR 16.5:1 speed, variable biodiesel + 80% Diesel + 100 ppm BaO Nano O2 smoke 2018a)
load Diesel additives ↑: CO2, NOx
Single cylinder, 4 S, RP: 5.2 kW, Constant 20% Azolla 20% Azolla biodiesel + 80% ↓: CO, HC, – (Kannan and Christraj,
1500 rpm, CR 16.5:1 speed, variable biodiesel + 80% Diesel + 100 ppm Bi2O3 Nano smoke 2018a)
load Diesel additives ↑: NOx
Single-cylinder, water-cooled, 4 S, RP: Constant Diesel 20% Azolla pinnata biodiesel ↓: NOx ↓: BTE (Narayanasamy and
5.2 kW, 1500 rpm, CR 16.5:1 speed, variable + 80% Diesel ↑: CO, HC, ↑: BSFC Jeyakumar, 2019)
load 20% Azolla biodiesel + 80% Smoke ↓: BSFC
Diesel + 100 ppm TiO2 Nano ↓: CO, ↑: BTE
additives Smoke
↑: HC, NOx
Kirloskar TV1, single cylinder, 4 S, RP: Constant Diesel 25% Azolla Microphylla ↓: NOx ↓: BTE (Thiruvenkatachari
5.2 kW, 1500 rpm, CR 17.5:1 speed, variable biodiesel + 75% Diesel ↑: CO, HC, et al., 2021)
load Smoke
Kirloskar, single cylinder, 4 S, RP: 3.7 kW, Constant Diesel 20% Azolla pinnata biodiesel ↓: HC, CO, ↓: BTE, EGT (Subramaniam et al.,
1500 rpm, CR 16.5:1 speed, variable + 80% Diesel Smoke, NOx ↑: BSFC, 2020)
load TFC,

11
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Table 3
Properties of Azolla species in comparison with diesel as per ASTM standards and EN standards (Bose, 2018; Prabakaran et al., 2021; Subramaniam et al., 2020;
Thiruvenkatachari et al., 2021).
Properties Unit Azolla filiculoides Azolla pinnata Azolla microphylla Diesel ASTM D6751 − 06 standard EN 14214 Standard

Cetane number – 51.3 51 51 47 > 47 > 51


Density at 15 ◦ C g/cc 0.870 0.863 0.854 0.834 0.860–0.900 0.860–0.900
Viscosity (40 ◦ C) cSt 5.75 4.3 5.15 2.5 1.9–6.0 3.5–5.0
Calorific value MJ/kg 43.85 40.68 38.11 45.5 – –
Flash point ◦
C 97 108 72 51 > 93 > 101
Pour point ◦
C – 3.1 -8 -21.2 – –
Cloud point ◦
C – 8.2 – -4.1 – –

Fig. 15. Processes used in phytoremediation of heavy metals.

Pb, Hg and Zn. Heavy metals negatively impact human health; hence radiations, α-glucuronic acid and pectin do not remove the nano­
HM pollution requires special consideration. Meanwhile, Co, Ni, Cu, Fe, particles. In this technique, reduction and adsorption were applied for
Mn, Zn and Mo are necessary for good plant development and meta­ recycling metallic ions and removing them from industrial wastewater.
bolism. The ratio among HM in a shoot (stem + leaves) to wastewater is Ghorbanzadeh Mashkani et al. (2009) explained the comparison be­
described as a biological accumulation factor (BAC). The bio­ tween the control and the presence of Sr & Cs on the medium of Azolla,
translocation coefficient (BTC) was calculated as the proportion of HM showing about 46.3% & 27.4% growth inhibition. To determine the
in Azolla shoot to Azolla roots. These variables were utilized to confirm binding ability of Sr and Cs, the experiment was conducted through a
the phytoextraction capacity of Azolla under consideration (Kumar Bio-sorption batch process. The best removal efficiency was obtained
et al., 2020; Sundararaman et al., 2021). Only a few amounts of litera­ when samples were treated with 2 M MgCl2 & 8 mM 30 ml H2O2 for
ture have been published to the depth of our knowledge on the biore­ 12 h at 7 pH and washed with NaOH solution for six hours.
mediation of heavy metal adsorption using Azolla. Pre-treatment shows that the surface of Azolla improves the biosorption
Bianchi et al. (2020) studied the removal of Al (III), Fe (III) and Cr techniques. The binding property of Sr & Cs on the surface of Azolla was
(VI) from treated wastewater using Azolla free-floating plants to un­ studied using FT-IR & micro-PIXE (Ghorbanzadeh Mashkani and Tajer
derstand the effectiveness of wastewater refining treatment used in a Mohammad Ghazvini, 2009).
surface flow constructed wetland. Fe and Al salts are widely used in the Tejada-Tovar et al. (2020) investigated the dead Azolla removes
clariflocculation process as a coagulant agent for wastewater treatment Pb2⁺, Cd2⁺, Ni2⁺ and Zn2⁺ relative to the second-order kinetics model. A
plants. Chromium is most probably found in industrial wastewaters, for higher adsorption capacity was obtained for activated Azolla and
example, textile industries. At laboratory conditions, 5 mg/L of plant non-activated Azolla. For the removal of metal ions using activated
concentration was exposed to the metals. Azolla shows the removal ef­ Azolla enthalpy (H) between 4.557 and 4.365 kcal/mol range & the
ficiencies of about 96% of Al, 92% of Fe, and Cr < 10% (Bianchi et al., entropy (S) was 1.006–2.290 cal/mol K. To remove the metal ions by
2020). Banach et al. (2020) fabricated the metallic Pb and Ag nano­ non-activated Azolla, the enthalpy (H) between the range of
particles from the ions using Azolla under microwave radiation. After 3.685–3.967 kcal/mol and entropy change (S) was between 0.933 and
five minutes of microwave reaction, the metallic Pb and Ag nano­ 2.440 cal/mol K ranges. For activated Azolla, higher adsorption capacity
particles were removed entirely from the contaminated solution, which to remove the metal ions by using an alkali such as NaCl: CaCl2: MgCl2
was present on the surface of Azolla. The size of lead and silver nano­ (in the molar ratio of 1:1:2) at 283–313 K was 1.431–1.272,
particles is 10–50 nm in a spherical shape. By using Mass balance data, 1.365–1.198, 1.173–0.990 & 1.291–0.981 mmol /g dry biomass. For
the Ag particles were found on the surface of Azolla. Under microwave non-activated Azolla, Qmax to remove heavy metals was obtained at

12
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

1.131–0.977, 1.212–0.931, 1.092–0.921, & 1.103–0.923 mmol/g dry Table 4


biomass. The living activated Azolla removes the heavy metals relative Utilization of Azolla for bioremediation process.
to first-order kinetics. During ten days period, the Azolla growth rate and Contaminant Parameters Yield Reference
uptake of HM were effective. The usage of Ca(NO3)2 increased the up­
Fe, Al, Cr Sample= 5 mg/L, Removal (Bianchi et al.,
take of heavy metals and growth. In the case of KNO3, the growth of mineralized with efficiency is 92%, 2020)
Azolla increased but decreased the HM uptake (Tejada-Tovar et al., HNO3 solution. 96%, and less
2020). Bind et al. (2018) studied the dried, milled Azolla, which removes than 10%.
98.2% of Au in industrial wastewater; gold from the plating industry Silver and The concentration of Maximum (Elmachliy et al.,
Lead the Ag+ and Pb2ᶧ ions adsorption 2011)
contains 5 mg of Au/lit in solution through a batch biosorption process. was 0.02 M. 5 min capacities of the
The adsorption capacity of gold by biomass is 98 mg/g. In diluted introduced to the Silver and lead
wastewater, 100% gold recovery is seen in a continuous flow column microwave oven. were 171 and
when dried biomass is used. In undiluted wastewater, a similar flow 109 mg/g
biomass.
column process linked to a two-step system of sulfide precipitation
Cs and Sr Treated: 2 M MgCl, Cs and Sr Ghorbanzadeh
shows 98% removal of Au containing 41 mg Au/l (Bind et al., 2018). 30 ml H2O2 8 mM for removal 195 and Mashkani et al.,
Khosravi et al. (2005) work on the Azolla growth and tolerance in 12 h. Washed: NaOH 212.1 mg/g dry, 2009)(
polluted mediums. The individual effect of Pb2⁺, Cd2⁺, Ni2⁺ & Zn2⁺ on sol, 6 h. pH 8&9. respectively. Ghorbanzadeh
Azolla growth were studied. Duration of 15 days, the Azolla of 20 g Mashkani and Tajer
Mohammad
grown on a nutrient solution containing metal ions of 4 mg/L each. In Ghazvini, 2009)
comparison to control, the presence of metal ions shows 25%, 42%, 31% Au Inoculated at 60 ◦ C for Batch: 98.2% (Umali et al., 2006)
& 17% inhibition of growth. One, two & four grams of NaCl per liter of 6 h and milled recovery
the medium decreases the removal of heavy metals in the range of 4–7%, 37 ◦ C for 48 h. Column: 95% on
day five and
20–24% & 40–55%. The addition of total dissolved solids (CaCO3) from
100% on day six.
50 to 300 ppm into the samples increased the growth of Azolla but Pb, Cd, Ni Grown on the nutrient Azolla growth up (Taghi Ganji et al.,
decreased the growth of the control sample (Khosravi et al., 2005). and Zn solution containing to 21.0%, 22.6%, 2005)
Taghi Ganji et al. (2005) studied the uptake of metals on the treated these metal ions, each 23.0% and
Azolla using H2O2 or MgCl2 in the batch biosorption experiment. Azolla in a concentration of 22.4% in Pb2ᶧ,
4 mg/L. 15 days. Cd2ᶧ, Ni2ᶧand Zn2ᶧ
collected from the rice field shows a maximum uptake capacity of 228,
solution.
62, 86 & 48 mg/g for Pb, Cu, Cd & Zn ions at optimal conditions. The Pb2ᶧ, Cd2ᶧ, NaOH at pH 10.5 Removal of Pb2ᶧ, (Khosravi et al.,
Azolla collected from the north part of Iran at Anzali International shows Ni2ᶧ and ± 0.2 and CaCl2/ Cd2ᶧ, Ni2ᶧ and 2005)
the uptake capacity of heavy metals was 124, 33, 58 & 34 mg/g under Zn2ᶧ MgCl2/NaCl with total Zn2ᶧ. In batch
concentration of 2 M. reactors 271,
similar conditions. The differences in uptake are due to the pollution of
111, 71 and
different areas. Recovery of HM from rice field Azolla was proceeded by 60 mg/g dry. In
NaCl & HCl desorbents of nearly 51–72% and 64–86% (Taghi Ganji fixed-bed
et al., 2005). Ahmady-Asbchin et al. (2011) work on Azolla was the reactors − 186,
removal efficiency of 86% & 100% of Au (III) from the initial solution of 95, 54 and
48 mg/g dry.
2–10 mg Au/lit, which increases with the increased concentration of Au
Gold (III) Studies performed 100% removal. (Antunes et al.,
(III). Azolla biomass was > 95% removal efficiencies at all concentra­ with hydrogen 2003)
tions from solutions measured. The Removal of Au at pH 2 was 42% and tetrachloroaurate (III)
at pH 3 & 4 was 63% & 73%. For pH 5 & 6 no temperature-dependence solution, at pH 2 in
range of 10–50 ◦ C.
removal. Umali et al. (2006), in this study, Azolla filiculoides (non-viable
Pb 4–8 mg/L biomass Pb removes up to (Sanyahumbi et al.,
biomass) remove Pb about 93 mg/g of biomass. The initial removal concentration at 93 mg/g of 1998)
concentration of Pb is 30% at a pH of 1.5. At 400 mg/L of Pb concen­ pH1.5 in temp range biomass.
tration, it decreases 30% of the initial Pb removal. About 90% of Pb of 10–50 ◦ C.
removal, 4–8 mg/L biomass concentration shows a small effect on Pb
removal at 10 ◦ C and 50 ◦ C (Ahmady-Asbchin et al., 2011). Table 4
can be used as a biofertilizer in various crops such as rice, wheat, taro,
summarizes the utilization of Azolla for the bioremediation process.
banana and tomatoes (York and Garden, 2016). Weeds are an un­
avoidable component of agricultural processes. Weeds are the most
7. Biofertilizer
significant impediment to higher yield in rice fields. Furthermore, if the
perennial weeds grow entrenched, the area may be unsuitable for
Biofertilizers enhance the accessibility to crops by improving the
agricultural cultivation (Allen and Vandever, 2012; Kamath et al.,
nutrient content of the soil. The main application of fertilizer is to
2020). Thus, weed management in rice paddy areas is critical for
supplement nitrogen and phosphate for the growth of plants (Nosheen
maximum yield. Many researchers have reported Azolla’s contribution
et al., 2021). Azolla act as a promising biofertilizer because of its high
as a biofertilizer and its potential to boost fertilizer efficiency in paddy
nitrogen-fixing content. Its ventral surface has a multi-branched
rice fields (Shen, 1985). Since 1927, the potential of Azolla to inhibit
rhizome that bears small leaves. It contains handing roots into water
other weeds has been discussed in Philippino’s literary research (Biswas
to absorb the nutrient contents directly (Roger, 1999). The leaves consist
et al., 2005). Weed growing is stopped whenever Azolla creates a dense,
of chlorophylls and a colorless lobe to supply buoyancy. Each lobe
nearly light-proof mat. There are possibly two techniques for this inhi­
contains a cavity that provides a microcosm environment with
bition. One of the most efficient is the light-starvation of immature weed
self-developed and defined. It behaves as a symbiotic unit association
seeds caused by sunlight obstruction. The other method would be the
when an energetic and metabolic reaction occurs (Adhikari et al., 2020).
physical restriction against weed seed emerging provided by a thick,
Azolla has been considered green manures in several developing coun­
interconnecting Azolla mat, which does not affect rice development
tries to fertilize the paddies and improve the yields, especially for rice
(Lumpkin and Plucknett, 1981).
cultivation shown in Fig. 16(a & b), which fixes nearly 40–60 Kg N/ha of
Vermicompost is a by-product of a decomposed process involving
rice crop (Rai et al., 2018). It has the property to multiply faster at very
several worm species shown in Fig. 16(c & d). It is an environmentally
high rates and covers the surface of water bodies; thus, it forms a thick
safe, non-toxic and preferable fertilizer resource for household
mat and helps in reducing the volatility of ammonia in the fields. Azolla

13
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Fig. 16. Morphology of the sporophytes of Azolla. (a) Round shape of Azolla filiculoides with chlorophyllous dorsal lobes(Ruano et al., 2016). (b) Azolla in a paddy
field at Bahour village, Pondicherry. (c) Vermicompost prepared from Azolla fillicaloids at household level (d) Paddy field on green manuring using Azolla fillicaloids.

gardening and organic farming (Indrani et al., 2019). It increases the nitrogen indicators, C: N and the rate of microbial respiration show
soil’s condition and aerates it naturally. Generally, the main ingredients maximum correlation (Yan et al., 2015).
are animal dung and sliced agricultural wastes (Piya et al., 2018). The Singh (2012) investigated the impact of incorporated supplements
inclusion of both leguminous and non-leguminous agricultural wastes the board rehearses on soil natural carbon (SOC) divisions, soil carbon
improves the quality of vermicompost. It also suggests that vermi­ (C) stockpiling, and grain efficiency was researched in winter wheat
composting of Azolla might be a helpful strategy to become a (Triticum aestivum) for two continuous seasons. Ripeness medicines were
value-added product, which is high in nutrients and could be employed NPK (Nitrogen, Phosphorus and Potassium) as suggested inorganic
locally in agricultural production (Najar and Khan, 2010). manure, NPK + cow dung, NPK + entire pieces of the green fertilizer
Azolla plays an important role to achieve nitrogen use efficiency due plant Sesbania aculeata, NPK + manure of Azolla caroliniana and NPK
to the higher potential for biological nitrogen fixation (BNF) in paddy + rice husk dust. NPK, through inorganic manure and in the mix with
rice fields. Nitrogen usage efficiency is improved by using Azolla bio­ natural corrections, expanded SOC and its dynamic and uninvolved
fertilizer; it increases rice yield and reduces nitrogen loss. RNA (25%), carbon portions. The use of organics with inorganic manures brought
FNA, RN (25%), CK, FNA or the five treatments are done in a three-year about more noteworthy soil carbon collection over inorganic compost
experimental field. Net economic benefit, Nitrogen use efficiency, rice alone. Higher centralization of microbial biomass carbon was recorded
yield and NH3 volatilization are evaluated (Yang et al., 2020). In RNA at NPK + cow dung and NPK + Sesbania aculeata. Azolla manure
and FNA, Azolla biofertilizer shows more recovery efficiency (69% and application with inorganic compost may be an excellent system for
59%) and provides higher nitrogen use efficiency (52% and 31%) than decreasing carbon dioxide (CO2) in the environment through expanded
farmer’s nitrogen (FN) Treatment (43% and 13%), which were done in banner leaf photosynthesis and arranging stable humified substances in
three years. Azolla biofertilizer is a promising tool for farmers to improve the dirt without trading off the grain efficiency. Grain yield was
nitrogen use efficiency, yield and reduce nitrogen loss (Yao et al., 2018). expanded by 27% because of NPK + Azolla fertilizer application con­
Kandel et al. (2020) studied that nitrogen fertilizer is more efficient for trasted with control (Singh, 2012).
higher grain yield and crop growth. The soil weights of Azolla filiculoides Nitrogen fertilizer is considered an organic fertilizer to increase food
compost are at 7.5, 2.5 or 5.0% (w/w). The N2 absorption is used to raise demand. Whereas, in other regions, it causes harmful effects on the
the yield of grain and possibly of other nutrients with Azolla filiculoides environment due to reducing nitrogen fertilizer compact food safety in
compost is considered a soil modification in rice cultivation, which some regions (Shaji et al., 2021). Industrial histamine binding protein
shows the good effect of Azolla compost on the growth of rice (Razavi­ (HBP) attains N-fertilizer from atmospheric nitrogen in an energy
pour et al., 2018). The development of a low input cropping system is concentrated process. The main work of nitrogen-fixing cyanobacte­
provided by Azolla filiculoides compost for the production of rice. rium; is used as a Semi-arid soil conditioner and organic fertilizer by
Microbial activity in soil and N and C transformation is controlled by recycling the nutrients from industrial waste (Yao et al., 2018). Nitrogen
the irrigation regime type under the significance of organic amendments from N₂ fixing cyanobacterium and phosphorous from the bone meal is
and drying rewetting alternatively. Alternative drying and wetting, used to enlarge the crop fertilization value of microbial biomass (Nas­
saving water, are also used to control the cycling, activity of microor­ cimento et al., 2019). Table 5 depicts the application of Azolla in
ganisms, soil-aggregate formation, carbon and nitrogen transformation biofertilizer.
and organic matter decomposition (Bagheri-Novair et al., 2020). AZ
compost and rice straw reduced the negative effect of drying rewetting
stress on the paddy soil. Compared to other measured carbon and

14
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Table 5 value-added products. The demand for Azolla is more because it contains
Studies for Azolla as a biofertilizer. high nitrogen fixation potential. The effects of Azolla are obtained using
Product Parameter Yield Reference some processes, such as torrefaction, hydrothermal liquefaction, pyrol­
ysis and gasification. The main application of Azolla is to produce
Biofertilizer on Different treatments: 56–80% (Kandel et al.,
Rice SN, T1, T2, T3, T4, T5, 2020) bio-diesel. KOH modified pyro chars, and raw are able to raise the
Production T6 value-added chemicals and reduce the amount of acid (Pirbazari et al.,
Biofertilizer Top soil has a pH Recovery (Yao et al., 2019). Biswas et al. (2017) investigated a fixed bed reactor for water
(H2O) of 7.35, and efficiency of 2018) hyacinth and pyrolysis of Azolla and sargassum tenerrimum at various
contains 26.6 g kg− 1 fertilizer N by
organic C, 2.09 g kg− 1 69% and 59%
temperatures of approximately 350–450 ◦ C. It is used to know the for­
total N, 0.93 g kg− 1 mational changes of different aquatic biomass on product’s nature and
total P, 121.3 mg kg− 1 product distribution at slow pyrolysis. Fossil fuels are replaced by using
available K and 17.7 bioenergy (or) biomass to be validated as a renewable energy source.
cmol kg− 1 CEC.
Naturally observed lignocellulosic biomass, higher photosynthetic effi­
Temperature: 80 ⁰C
(Grain and straw) ciency and faster growth are given by aquatic biomass. Sargassum ten­
Properties of Require 50% sunlight, yield of 37.8 tons/ (Lumpkin and errimum shows a higher bio-oil yield and conversion. 43 wt% bio-oil can
Azolla ph: 4.5 – 7, ha fresh weight Plucknett, also show a relatively low rate of pyrolysis (Biswas et al., 2017).
temperature: 20–30 ⁰C, containing 2.78 1981) Muradov et al., examined the possibility of dual implementation of
salinity of 1.3% tons dry weight of
A. pinnata
Azolla and duckweed plants for the development of renewable fuels and
Production of Acidic (pH 3.5–5.0), Nostoc biomass (Nascimento wastewater management. These microphytes used the important
organic rich in organic matter, attained > 50% of et al., 2019) wastewater nutrition phosphorous and ammonium as the basic principle
fertilizer and Ca, K, Mg and S and the dry weight for optimizing compositions of wastewater effluents. Assessment of
soil low in N and P.
pyrolysis products has shown that Azolla algae give the same range of
conditioner Dilution of 0.4% (v/v)
Effects of soil Soil Salinity pH ˂8.5 – (Yan et al., bio-oils containing a wide range of petrochemicals, including C10 - C21
salinity and 2015) straight-chain alkanes, that can be effectively utilized as diesel fuel
water content substitute or else glycerin free biofuel. Duckweed pyrolysis provides a
on soil unique range of bio-oil elements that can be used to prepare green
microbes
gasoline. Pure diesel fuel has been used in the existing approach,
including catalyzed hydrodeoxygenation (Muradov et al., 2014). Bose
8. Bio-oil (Bose, 2018) Suggested that macroalgae were promising sources of
biofuel. Growth of evaluation was conducted for Azolla pinnata, and
Bio-oil is one of the most appealing liquid biofuels (bio-ethanol, bio- biofuel produced by transesterification was done. The suitability of
diesel and bio-oil) derived from the pyrolysis process because of its biofuel from Azolla was identified with FTIR and GCMS analysis. Ther­
carbon neutrality nature, as shown in Fig. 17(b). As compared to stan­ mophysical properties obtained for biodiesel were noted as close to
dard fossil fuels, the usage of bio-oil produces less nitrogen dioxide and diesel fuel. Salehzadeh et al. (2014) Examined chloroform-methanol
sulfur dioxide emissions (Terry et al., 2021). Since bio-oil is compatible solvent (2:1 v/v) in the Soxhlet extraction method to collect crude oil
with most current equipment, safety regulations, and pumping systems, from cold-dried Azolla fern shown in Fig. 17(a). Acid transesterification
it is extremely easy to store and transport than charcoal and biogas was used to convert the fatty acid and triglycerides into the FAME. The
(Rabiu et al., 2018). Bio-oil is a perplexing combination of over 400 conversion of FAME was analysed with the GC-MS test. The existence of
different oxygenated chemicals with various functional groups. Light palmitic acid, myristic acid, stearic acid, oleic acid, linoleic acid, and
fluid solvent oxygenates, phenolics, anhydyosugars, furanics, and sugars erucic acid confirms that biodiesel could be prepared from Azolla algae.
are among the families of these combinations (Drugkar et al., 2022; It was effectively an economical source due to its abundant availability
Terry et al., 2021). (Salehzadeh et al., 2014). Hemalatha et al. (2020) The deoiled Azolla
Pirbazari et al. (2019) investigated the effect of Mg-Ni-Mo/MPC, pinnata biomass (DAB) substrate was analysed to operate microbial fuel
pyro char, and modified pyro on the production of bio-oil and other cells and acted as an electrode. The anode was manufactured with

Fig. 17. (a) Dried Azolla biomass (b) Bio-oil from Azolla deoiled cake.

15
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

biochar acquired from pyrolysis of DAB at 800 ◦ C, whereas the reduction massive volumes of CO2 in the atmosphere, which is a need for carbon
of sugars by acid pre-treatment after DAB hydrolysis was used as a credit. Dual cropping can reduce greenhouse gas emissions such as CH4
substrate. Post-pyrolyzed biochar was analysed for elemental and and N2O from agriculture. In an irrigated rice ecosystem, Azolla double
structural functionality by Raman spectroscopy, SEM and XRD, while crops reduced CH4 pollution by 40% compared to urea alone while
the reduction in sugar from hydrolyzed DAB was evaluated for its stimulating CH4 oxidation (Kollah et al., 2016). Coconut based inte­
composition. The results suggest that a voltage of 382 mV at a given 3 g grating farming for the climate-smart model were studied for the best
COD/L decreased 65.6% of chemical oxygen demand (COD) in closed management of socioeconomic and environmental aspects (Sudha et al.,
circuit operation (Hemalatha et al., 2020). Narayanasamy et al., 2019 2021). The Azolla was included in this model as a major player to replace
Studied the performance and emission characteristics of the CI engine inorganic fertilizer. Munyaka et al. (2020) reported the benefits of
with the inclusion of TiO2 nano additive in the Azolla methyl ester. The economic and environmental benefits of co-feeding of Azolla and bio­
amount of bio-oil extraction from the Soxhlet apparatus was found to be char prepared from poultry litters. This combination has increased rice
higher than the hydraulic pressing method. The transesterification grain production by 27.3–75.0% and reduced the CH4 emission by
process was used to produce biodiesel, and the properties were tested 27.3–75.0% and N2O by 81.8–97.7% (Munyaka et al., 2020).
according to ASTM standards (Narayanasamy and Jeyakumar, 2019). Maham et al. investigated the environmental performances and
vitamin c content of the organic greenhouse tomatoes grown with bio­
9. Environmental and economic assessment aspects of Azolla fertilizers obtained from Azolla, a nitrogen-fixing species that provides
nutrients to plants for tomato cultivation and also water stress levels.
The little floating fern has a wide spectrum of environmental and GHG emission for each tonne of natural greenhouse tomato was
economic benefits were shown in Fig. 18. The unconditional growth and 5.47 × 102 kg CO2 eq., which demonstrates that using natural fertilizers
its resilient property on weed were found most attractive for paddy depending on nitrogen-fixing plants (Azolla) in greenhouse production
cultivation, in addition to nitrogen-fixing and oxygen supply to roots results in a significant decrease in GHG emission when related to pro­
(Pawan and Singh, 2015). The entire life cycle of this tiny fern shares ducing in natural greenhouses solely based on manure. As a result, the
ample benefits such as organic manure, bioremediation of hazardous utilization of nitrogen-fixing plants may be a viable approach for
pollutants and restoration of saline soil, feed supplement for animals, decreasing environmental impacts caused by greenhouse products,
fish and duck etc.; it fixes nitrogen, enriches organic carbon and con­ particularly the phenomena of climate change and global warming
tributes to the reduction of greenhouse gases emission, it also used for (Maham et al., 2020). Kollah et al. (2016) reviewed the sustainable
the production of hydrogen and biogas. In addition to environmental opportunities of Azolla with reference to nitrogen-fixing, bio-remedia­
benefits, several articles reported significant economic benefits, espe­ tion potentials, and its ability to reduce the emission of greenhouse
cially in the cultivation of paddy and feed for livestock (Hyde et al., gases. This article highlighted the coexisting economic benefits with
2019). environmental benefits (Kollah et al., 2016). Kumar et al., highlighted
The nitrogen fixation capacity of the cyanobacterial symbiont ranges the role of Azolla in bringing prospective changes in salinity affected
between 30 and 60 kg N ha − 1, indicating that Azolla is a key biological regions. The Azolla-Anabaena symbiotic system has significantly sup­
nitrogen resource for farming and the livestock industries. Paddy culti­ ported the nitrogen economy and the productivity of nitrogen-limited
vation accounts for approximately 40–50% cost of fertilizers, and the soil. This study summarized the development and application of
application of Azolla reduces the cost significantly. The increasing salt-resistant Azolla strains in the recreation of farming practices in
concern for food in the perspective of health and environmental con­ salt-affected areas (Kumar et al., 2009). Saha et al. (2017) explained
servation encourages the application of clean green fertilizers. Gener­ biological nitrogen fixation for sustainability in agricultural practices.
ally, organic fertilizers limit their application due to the high volume to This study substantiated the symbiotic response of Azolla, which favored
weight ratio, but the rich nutrient content in Azolla made it feasible for the economic and environmental benefits (Saha, 2017; Bhattacharyya
the extraction of nutrients both economically and technically (Maham and Basak, 2017). Xu et al. (2017) conducted three years field experi­
et al., 2020). The organic manure from Azolla can be produced locally, ment on dual cropping of rice and Azolla. The application of Azolla as a
which indicates a good improvement in socio-economic growth, biore­ biofertilizer was compared with traditional inorganic N- fertilizers usage
mediation of hazardous pollutants from the agricultural output, and (400 kg N ha− 1 a− 1) and with minimal use (200 kg N ha− 1 a− 1). The
climate change to conserve biodiversity and the environment. Azolla has study results were promising in the reduction of methane emission
the potential to minimize the amount of energy required for fertilizer without compromising the yield, it is observed that Azolla has influenced
manufacturing as well as the ecological effects associated with energy the factors such as dissolved oxygen and soil redox potentials which
generation. The leaf structure of Azolla has developed to offer a micro­ contribute the methane emission in the paddy field (Xu et al., 2017). Yao
environment for nitrogen-fixation filament bacteria A.Azolla, which et al. (2018)(a) observed a 3-year experimental study on Azolla based
forms heterocysts. This would be the key to Azolla’s capacity to absorb biofertilizers with different usage practices of inorganic fertilizers,

Fig. 18. Economic and Environmental benefits of Azolla.

16
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

claiming that Azolla based biofertilizers for replacing 25% of urea N The biofertilizer obtained from Azolla reduces the inorganic fertilizer
render economically attractive options for farmers. The studies also aver significantly. The dual growth of paddy and Azolla ensures optimized
that the Azolla based biological nitrogen-fixing system has a better resource utilization, sustainable management, and use of natural re­
application in the utilization of nitrogen content in the soil. sources. The application of Azolla-based fertilizers reduces greenhouse
gas emissions from paddy fields. The Azolla protects the ecosystem from
10. Azolla for achieving sustainable development goals invasive species; it is also used for bioremediation and wastewater
treatment (Bocchi and Malgioglio, 2010).
Azolla is widely helping to achieve sustainable development goals by
reducing poverty by supporting salinity, and drought-resilient farming is 11. Conclusion and future perspective
depicted in Fig. 19. The accumulation of salts in the soil worsens
farming. The Intergovernmental science-policy platform report on The high growth rates of Azolla reduce the environmental risks, and
biodiversity explicit the impact of salinity in agriculture. Nearly 190 it is a cost-effective method for developing wetlands. The bioremedia­
million acres have been lost altogether, 150 million acres have been tion method is trouble-free and has a low production cost. The Azolla
destroyed, and 2.5 billion have been affected by salinity (Mukho­ biomass can be used as an effective biosorbent for lowering concentra­
padhyay et al., 2021). It helps sustainable food production to feed tion in polluted water and effluents. Azolla experienced low toxicity
humans & livestock. Azolla reduces the water evaporation in paddy from the investigated heavy metals. The bio-based heavy metal removal
fields and optimizes the water usage in paddy cultivation. (Miranda efficiency depended on the reaction time, weight, pH and temperature.
et al., 2016) Studies reported the application of Azolla in renewable The removal efficiency for Azolla is more than 95% of organic com­
energy production such as biodiesel, biogas and hydrogen production. pounds. Thus, Azolla is an ideal source for polishing wastewater. After

Fig. 19. Potential of Azolla in achieving SDGs.

17
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

bioremediation, the end product of Azolla can be converted into many removal: sorbent preparation, characterization, regeneration and cost estimation.
Geol. Ecol. Landsc. 2, 61–72. https://doi.org/10.1080/24749508.2018.1452460.
bioproducts; one primary product is bio-oil. The comparison of present
Biswas, B., Singh, R., Krishna, B.B., Kumar, J., Bhaskar, T., 2017. Pyrolysis of azolla,
oils for biodiesel and bio-oil content associated with Azolla shows its sargassum tenerrimum and water hyacinth for production of bio-oil. Bioresour.
suitability as biodiesel. The future feasibility of algae biodiesel pro­ Technol. 242, 139–145. https://doi.org/10.1016/j.biortech.2017.03.044.
duction needs to address three major issues: environmental conse­ Biswas, M., Parveen, S., Shimozawa, H., Nakagoshi, N., 2005. Effects of Azolla species on
weed emergence in a rice paddy ecosystem. Weed Biol. Manag. 5, 176–183. https://
quences, carbon balance and cost of production. In addition, appropriate doi.org/10.1111/j.1445-6664.2005.00177.x.
algal fuel additives that considerably increase engine efficiency and Bocchi, S., Malgioglio, A., 2010. Azolla-anabaena as a biofertilizer for rice paddy fields in
reduce emission parameters require further investigation using organic the po valley, a temperate rice area in northern Italy. Int. J. Agron. 2010, 1–5.
https://doi.org/10.1155/2010/152158.
chemistry and nanotechnology. This can make the properties of algal Bose, N., 2018. Production and characterization of biodiesel using 34, 1833–1838.
biofuels identical to those of conventional fossil fuels. Azolla biofertilizer Briffa, J., Sinagra, E., Blundell, R., 2020. Heavy metal pollution in the environment and
has the capacity to absorb phosphorus from soil and accumulate heavy their toxicological effects on humans. Heliyon 6. https://doi.org/10.1016/j.
heliyon.2020.e04691.
metals. In this aspect, the paddy field system seems to be an intriguing Drugkar, K., Rathod, W., Sharma, T., Sharma, A., Joshi, J., Pareek, V.K., Ledwani, L.,
application because colossal water consumption and repetitive mono­ Diwekar, U., 2022. Advanced separation strategies for up-gradation of bio-oil into
culture can lead to the deposition of pollutants in the soil over time. Still, value-added chemicals: a comprehensive review. Sep. Purif. Technol. 283, 120149
https://doi.org/10.1016/j.seppur.2021.120149.
less attention is given to evaluating the efficacy of double-cropping of Elmachliy, S., Chefetz, B., Tel-Or, E., Vidal, L., Canals, A., Gedanken, A., 2011. Removal
Azolla (with rice) in greenhouse cultivation operations to enhance crop of silver and lead ions from water wastes using Azolla filiculoides, an aquatic plant,
and soil properties. Effective extension techniques are also required to which adsorbs and reduces the ions into the corresponding metallic nanoparticles
under microwave radiation in 5 min. Water Air. Soil Pollut. 218, 365–370. https://
promote the Azolla as a bio-fertilizers with additional advantages. The
doi.org/10.1007/s11270-010-0650-3.
Azolla fern protein contains amino acids that could be employed as food FAO, 1978. China: Azolla propagation and Small-Scale biogas technology. FAO Soils
additives and flavor boosters. Furthermore, the Azolla biomass included Bull. 81.
caffeic acid and eicosapentaenoic acid, which have medicinal value. Allen, A.W., Vandever, M.W., 2012. Conservation Reserve Program ( CRP) contributions
to wildlife habitat, management issues, challenges and policy choices — An
Annotated Bibliography: U.S. Geological Survey Scientific Investigations Report
Declaration of Competing Interest 2012 – 5066. Sci. Investig. Repotz 185p.
Andreo-Martínez, P., Ortiz-Martínez, V.M., García-Martínez, N., de los Ríos, A.P.,
Hernández-Fernández, F.J., Quesada-Medina, J., 2020. Production of biodiesel
The authors declare that they have no known competing financial under supercritical conditions: state of the art and bibliometric analysis. Appl.
interests or personal relationships that could have appeared to influence Energy 264, 114753. https://doi.org/10.1016/j.apenergy.2020.114753.
the work reported in this paper. Ansari, A.A., Naeem, M., Gill, S.S., AlZuaibr, F.M., 2020. Phytoremediation of
contaminated waters: an eco-friendly technology based on aquatic macrophytes
application. Egypt. J. Aquat. Res. 46, 371–376. https://doi.org/10.1016/j.
Acknowledgment ejar.2020.03.002.
Antunes, A.P.M., Nightingale, D.S.L., Maclear, R.P.A., Duncan, J.R., 2003. Development
of bioreactor systems for the treatment of heavy metal containing effluents: WRC
The authors gratefully acknowledge the financial support of SERB Report No 845/1/03.
(Science & Engineering Research Board), INDIA (Grant no. ECR/2017/ Arutyunov, V.S., Lisichkin, G.V., 2017. Energy resources of the 21st century: problems
001038/2017-2020 & SB/EMEQ-006/2014) to carry out this review and forecasts. Can renewable energy sources replace fossil fuels? Russ. Chem. Rev.
86, 777–804. https://doi.org/10.1070/rcr4723.
work. Babu, S.M.O.F., Hossain, M.B., Rahman, M.S., Rahman, M., Ahmed, A.S.S., Hasan, M.,
Rakib, A., Emran, T., Bin, Xiao, J., 2021. Phytoremediation of toxic metals: a
References sustainable green solution for clean environment. Appl. Sci. 1–34.
Bagheri-Novair, S., Mirseyed Hosseini, H., Etesami, H., Razavipour, T., Asgari Lajayer, B.,
Astatkie, T., 2020. Short-term soil drying–rewetting effects on respiration rate and
Abd El-Aal, A.A.M., 2022. Anabaena-azollae, significance and agriculture application: a
microbial biomass carbon and phosphorus in a 60-year paddy soil. 3 Biotech 10,
case study for symbiotic cyanobacterium. In: Pratap Singh, Raghvendra,
1–11. https://doi.org/10.1007/s13205-020-02486-w.
Bhattacharjee, Kaushik, Manchanda, Geetanjali, Panosyan, Hovik (Eds.), Microbial
Banach, A.M., Kuźniar, A., Grządziel, J., Wolińska, A., 2020. Azolla filiculoides L. As a
Syntrophy-Mediated Eco-enterprising. Academic Press, pp. 1–14. https://doi.org/
source of metal-tolerant microorganisms. PLOS One 15, 1–25. https://doi.org/
10.1016/B978-0-323-99900-7.00006-7.
10.1371/journal.pone.0232699.
Abusweireh, R.S., Rajamohan, N., Vasseghian, Y., 2022. Enhanced production of
Bhattacharyya, P.K., Basak, N., 2017. Biological nitrogen fixation for sustainable
biodiesel using nanomaterials: a detailed review on the mechanism and influencing
agriculture. https://doi.org/10.1007/978-981-10-5343-6.
factors. Fuel 319, 123862. https://doi.org/10.1016/J.FUEL.2022.123862.
Bhuyar, P., Sundararaju, S., Rahim, M.H.A., Ramaraj, R., Maniam, G.P., Govindan, N.,
Adane, T., Adugna, A.T., Alemayehu, E., 2021. Textile industry effluent treatment
2021. Microalgae cultivation using palm oil mill effluent as growth medium for lipid
techniques. J. Chem. 2021. https://doi.org/10.1155/2021/5314404.
production with the effect of CO2 supply and light intensity. Biomass Convers.
Adhikari, K., Bhandari, S., Acharya, S., 2020. An overview of azolla in rice production: a
Biorefin. 11, 1555–1563. https://doi.org/10.1007/s13399-019-00548-5.
review. Rev. Food Agric. 2, 04–08. https://doi.org/10.26480/rfna.01.2021.04.08.
Brouwer, P., van der Werf, A., Schluepmann, H., Reichart, G.J., Nierop, K.G.J., 2016.
Ahmad, M.S., Cheng, C.K., Bhuyar, P., Atabani, A.E., Pugazhendhi, A., Chi, N.T.L.,
Lipid yield and composition of azolla filiculoides and the implications for biodiesel
Witoon, T., Lim, J.W., Juan, J.C., 2021. Effect of reaction conditions on the lifetime
production. Bioenergy Res. 9, 369–377. https://doi.org/10.1007/s12155-015-9665-
of SAPO-34 catalysts in methanol to olefins process – a review. Fuel 283. https://doi.
3.
org/10.1016/j.fuel.2020.118851.
Brouwer, P., Schluepmann, H., Nierop, K.G.J., Elderson, J., Bijl, P.K., van der Meer, I., de
Ahmady-Asbchin, S., Mohammadi, M., Bahrami, A., Monfared, A.L., Jafari, N., 2011.
Visser, W., Reichart, G.J., Smeekens, S., van der Werf, A., 2018. Growing Azolla to
Batch studies on the removal of Ni (II) from aqueous solution by Azolla filiculoides.
produce sustainable protein feed: the effect of differing species and CO2
Afr. J. Biotechnol. 10, 7427–7431. https://doi.org/10.4314/ajb.v10i38.
concentrations on biomass productivity and chemical composition. J. Sci. Food
Alam, F., Mobin, S., Chowdhury, H., 2015. Third generation biofuel from Algae. Procedia
Agric. 98, 4759–4768. https://doi.org/10.1002/jsfa.9016.
Eng. 105, 763–768. https://doi.org/10.1016/j.proeng.2015.05.068.
Chisti, Y., 2007. Biodiesel from microalgae. Biotechnol. Adv. 25, 294–306. https://doi.
Al-Baldawi, I.A., Abdullah, S.R.S., Anuar, N., Hasan, H.A., 2018. Phytotransformation of
org/10.1016/j.biotechadv.2007.02.001.
methylene blue from water using aquatic plant (Azolla pinnata). Environ. Technol.
Chittora, D., Meena, M., Barupal, T., Swapnil, P., 2020. Cyanobacteria as a source of
Innov. 11, 15–22. https://doi.org/10.1016/j.eti.2018.03.009.
biofertilizers for sustainable agriculture. Biochem. Biophys. Rep. 22, 100737 https://
Ali, H., Khan, E., Ilahi, I., 2019. Environmental chemistry and ecotoxicology of
doi.org/10.1016/j.bbrep.2020.100737.
hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation.
Choi, Y.Y., Patel, A.K., Hong, M.E., Chang, W.S., Sim, S.J., 2019. Microalgae bioenergy
J. Chem. 2019. https://doi.org/10.1155/2019/6730305.
with carbon capture and storage (BECCS): an emerging sustainable bioprocess for
Bhuyar, P., Yusoff, M.M., Rahim, M.H.A., Sundararaju, S., Maniam, G.P., Govindan, N.,
reduced CO2 emission and biofuel production. Bioresour. Technol. Rep. 7, 100270
2020. Effect of plant hormones on the production of biomass and lipid extraction for
https://doi.org/10.1016/j.biteb.2019.100270.
biodiesel production from microalgae chlorella Sp. J. Microbiol. Biotechnol. Food
Dahlke, S., Sterling, J., Meehan, C., 2021. Policy and market drivers for advancing clean
Sci. 9, 671–674. https://doi.org/10.15414/JMBFS.2020.9.4.671-674.
energy. In: Kalam Azad, Abdul (Ed.), Advances in Clean Energy Technologies.
Bianchi, E., Biancalani, A., Berardi, C., Antal, A., Fibbi, D., Coppi, A., Lastrucci, L.,
Elsevier Inc. https://doi.org/10.1016/b978-0-12-821221-9.00012-8.
Bussotti, N., Colzi, I., Renai, L., Scordo, C., Del Bubba, M., Gonnelli, C., 2020.
Dahman, Y., Syed, K., Begum, S., Roy, P., Mohtasebi, B., 2019. Biofuels: Their
Improving the efficiency of wastewater treatment plants: Bio-removal of heavy-
Characteristics and Analysis, Biomass, Biopolymer-Based Materials, and Bioenergy:
metals and pharmaceuticals by Azolla filiculoides and Lemna minuta. Sci. Total
Construction, Biomedical, and Other Industrial Applications. Elsevier Ltd,. https://
Environ. 746, 141219 https://doi.org/10.1016/j.scitotenv.2020.141219.
doi.org/10.1016/B978-0-08-102426-3.00014-X.
Bind, A., Goswami, L., Prakash, V., 2018. Comparative analysis of floating and
submerged macrophytes for heavy metal (copper, chromium, arsenic and lead)

18
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Das, M., Rahim, F.I., Hossain, M.A., 2018. Evaluation of fresh Azolla pinnata as a low- emission characteristics study. Fuel 311, 122621. https://doi.org/10.1016/J.
cost supplemental feed for thai silver barb Barbonymus gonionotus. Fishes 3, 1–11. FUEL.2021.122621.
https://doi.org/10.3390/fishes3010015. Khan, M.A.H., Bonifacio, S., Clowes, J., Foulds, A., Holland, R., Matthews, J.C.,
David, C., Ganduri, J., Ragunathan, V., Natarajan, R., 2021. Characterization of pellets Percival, C.J., Shallcross, D.E., 2021. Investigation of biofuel as a potential
manufactured from plant waste and farm waste residues blended with distillery renewable energy source. Atmosphere 12. https://doi.org/10.3390/
sludge as a prospective alternative fuel source. Appl. Nanosci. https://doi.org/ atmos12101289.
10.1007/s13204-021-01982-6. Khan, S., Siddique, R., Sajjad, W., Nabi, G., Hayat, K.M., Duan, P., Yao, L., 2017.
De Benedetti, F., del, C., Zamaloa, M., Gandolfo, M.A., Cúneo, N.R., 2018. Heterosporous Biodiesel production from algae to overcome the energy crisis. HAYATI J. Biosci. 24,
ferns from patagonia: the case of azolla. In: Krings, Michael, Rubén Cúneo, Néstor, 163–167. https://doi.org/10.1016/j.hjb.2017.10.003.
Harper, Carla J., Rothwell, Gar W. (Eds.), Transformative Paleobotany: Papers to Khosravi, M., Rakhshaee, R., Ganji, M.T., 2005. Pre-treatment processes of Azolla
Commemorate the Life and Legacy of Thomas N. Taylor. Academic Press, filiculoides to remove Pb(II), Cd(II), Ni(II) and Zn(II) from aqueous solution in the
pp. 361–373. batch and fixed-bed reactors. J. Hazard. Mater. 127, 228–237. https://doi.org/
Dohaei, M., Karimi, K., Rahimmalek, M., Satari, B., 2020. Integrated biorefinery of 10.1016/j.jhazmat.2005.07.023.
aquatic fern Azolla filiculoides for enhanced extraction of phenolics, protein, and Kochi, L.Y., Freitas, P.L., Maranho, L.T., Juneau, P., Gomes, M.P., 2020. Aquatic
lipid and methane production from the residues. J. Clean. Prod. https://doi.org/ macrophytes in constructed wetlands: a fight against water pollution. Sustainability
10.1016/j.jclepro.2020.123175. 12, 1–21. https://doi.org/10.3390/su12219202.
Gholizadeh, A.M., Zarei, M., Ebratkhahan, M., Hasanzadeh, A., Vafaei, F., 2020. Removal Kollah, B., Patra, A.K., Mohanty, S.R., 2016. Aquatic microphylla Azolla: a perspective
of Phenazopyridine from wastewater by merging biological and electrochemical paradigm for sustainable agriculture, environment and global climate change.
methods via Azolla filiculoides and electro-Fenton process. J. Environ. Manag. 254, Environ. Sci. Pollut. Res. 23, 4358–4369. https://doi.org/10.1007/s11356-015-
109802 https://doi.org/10.1016/j.jenvman.2019.109802. 5857-9.
Ghorbanzadeh Mashkani, S., Tajer Mohammad Ghazvini, P., 2009. Biotechnological Konur, O., 2020. The scientometric analysis of the research on the algal bioremediation.
potential of Azolla filiculoides for biosorption of Cs and Sr: application of micro-PIXE Handb. Algal Sci. Technol. Med 607–627. https://doi.org/10.1016/b978-0-12-
for measurement of biosorption. Bioresour. Technol. 100, 1915–1921. https://doi. 818305-2.00038-3.
org/10.1016/j.biortech.2008.10.019. Kour, D., Rana, K.L., Yadav, A.N., Yadav, N., Kumar, M., Kumar, V., Vyas, P.,
Goala, M., Yadav, K.K., Alam, J., Adelodun, B., Choi, K.S., Cabral-Pinto, M.M.S., Dhaliwal, H.S., Saxena, A.K., 2020. Microbial biofertilizers: bioresources and eco-
Hamid, A.A., Alhoshan, M., Ali, F.A.A., Shukla, A.K., 2021. Phytoremediation of friendly technologies for agricultural and environmental sustainability. Biocatal.
dairy wastewater using Azolla pinnata: application of image processing technique Agric. Biotechnol. 23, 101487 https://doi.org/10.1016/j.bcab.2019.101487.
for leaflet growth simulation. J. Water Process Eng. 42, 102152 https://doi.org/ Kumar, S., Diksha, Sindhu, S.S., Kumar, R., 2022. Biofertilizers: an ecofriendly
10.1016/j.jwpe.2021.102152. technology for nutrient recycling and environmental sustainability. Curr. Res.
Golzary, A., Hosseini, A., Saber, M., 2021. Azolla filiculoides as a feedstock for biofuel Microb. Sci. 3, 100094 https://doi.org/10.1016/j.crmicr.2021.100094.
production: cultivation condition optimization. Int. J. Energy Water Resour. 5, Kumar, V., Nanda, M., Joshi, H.C., Singh, A., Sharma, S., Verma, M., 2018. Production of
85–94. https://doi.org/10.1007/s42108-020-00092-3. biodiesel and bioethanol using algal biomass harvested from fresh water river.
Hashemloian, B.D., Azimi, A.A., 2009. Alien and exotic Azolla in northern Iran. Afr. J. Renew. Energy 116, 606–612. https://doi.org/10.1016/j.renene.2017.10.016.
Biotechnol. 8, 187–190. https://doi.org/10.5897/AJB2009.000-9034. Kumar, V., Kumar, Piyush, Singh, J., Kumar, Pankaj, 2020. Potential of water fern
Hemalatha, M., Sravan, J.S., Min, B., Venkata Mohan, S., 2020. Concomitant use of (Azolla pinnata R.Br.) in phytoremediation of integrated industrial effluent of
Azolla derived bioelectrode as anode and hydrolysate as substrate for microbial fuel SIIDCUL, Haridwar, India: removal of physicochemical and heavy metal pollutants.
cell and electro-fermentation applications. Sci. Total Environ. https://doi.org/ Int. J. Phytoremediat. 22, 392–403. https://doi.org/10.1080/
10.1016/j.scitotenv.2019.135851. 15226514.2019.1667950.
Hoang, A.T., 2021. Combustion behavior, performance and emission characteristics of Kumar, V., Tripathi, B.D., Kim, K., 2009. Removal and accumulation of mercury by
diesel engine fuelled with biodiesel containing cerium oxide nanoparticles: a review. aquatic macrophytes from an open cast coal mine effluent 172, 749–754. https://
Fuel Process. Technol. 218, 106840 https://doi.org/10.1016/j.fuproc.2021.106840. doi.org/10.1016/j.jhazmat.2009.07.059.
Hyde, K.D., Xu, J., Rapior, S., Jeewon, R., Lumyong, S., 2019. The amazing potential of Kurniawan, S.B., Ahmad, A., Said, N.S.M., Imron, M.F., Abdullah, S.R.S., Othman, A.R.,
fungi: 50 ways we can exploit fungi industrially. Fungal Divers. 97, 1–136. https:// Purwanti, I.F., Hasan, H.A., 2021. Macrophytes as wastewater treatment agents:
doi.org/10.1007/s13225-019-00430-9. nutrient uptake and potential of produced biomass utilization toward circular
Ilyas, M., Ahmad, W., Khan, H., Yousaf, S., Yasir, M., Khan, A., 2019. Environmental and economy initiatives. Sci. Total Environ. 790, 148219 https://doi.org/10.1016/j.
health impacts of industrial wastewater effluents in Pakistan: a review. Rev. Environ. scitotenv.2021.148219.
Health 34, 171–186. https://doi.org/10.1515/reveh-2018-0078. Luiza Astolfi, A., Rempel, A., Cavanhi, V.A.F., Alves, M., Deamici, K.M., Colla, L.M.,
Indrani, Y., Abdullah, R., Ansari, A., Ori, L., 2019. Vermicomposting of different organic Costa, J.A.V., 2020. Simultaneous saccharification and fermentation of Spirulina sp.
materials using the epigeic earthworm Eisenia foetida. Int. J. Recycl. Org. Waste and corn starch for the production of bioethanol and obtaining biopeptides with high
Agric. 8, 23–36. https://doi.org/10.1007/s40093-018-0225-7. antioxidant activity. Bioresour. Technol. 301, 122698 https://doi.org/10.1016/j.
Islam, M.M., Hasanuzzaman, M., 2020. Introduction to energy and sustainable biortech.2019.122698.
development. Energy Sustain. Dev. Demand, Supply, Convers. Manag 1–18. https:// Lumpkin, T.A., Plucknett, D.L., 1981. Azolla, a low cost aquatic green manure for
doi.org/10.1016/B978-0-12-814645-3.00001-8. agricultural crops. Ctries 107–124.
Islam, S., 2020. A study on the solutions of environment pollutions and worker’s health Mahajan, P., Kaushal, J., 2018. Role of phytoremediation in reducing cadmium toxicity
problems caused by textile manufacturing operations. Biomed. J. Sci. Tech. Res. 28 in soil and water. J. Toxicol. 2018. https://doi.org/10.1155/2018/4864365.
https://doi.org/10.26717/bjstr.2020.28.004692. Maham, S.G., Rahimi, A., Subramanian, S., Smith, D.L., 2020. The environmental
Jacob, A., Ashok, B., Alagumalai, A., Chyuan, O.H., Le, P.T.K., 2021. Critical review on impacts of organic greenhouse tomato production based on the nitrogen-fixing plant
third generation micro algae biodiesel production and its feasibility as future (Azolla). J. Clean. Prod. 245. https://doi.org/10.1016/j.jclepro.2019.118679.
bioenergy for IC engine applications. Energy Convers. Manag. 228, 113655 https:// Mahmood, H., Alkhateeb, T.T.Y., Furqan, M., 2020. Industrialization, urbanization and
doi.org/10.1016/j.enconman.2020.113655. CO2 emissions in Saudi Arabia: asymmetry analysis. Energy Rep. 6, 1553–1560.
Jayakumar, S., Bhuyar, P., Pugazhendhi, A., Rahim, M.H.A., Maniam, G.P., Govindan, N., https://doi.org/10.1016/j.egyr.2020.06.004.
2021. Effects of light intensity and nutrients on the lipid content of marine microalga Mahmud, M.S., Chong, K.P., 2021. Formulation of biofertilizers from oil palm empty fruit
(diatom) Amphiprora sp. for promising biodiesel production. Sci. Total Environ. 768, bunches and plant growth-promoting microbes: a comprehensive and novel
145471 https://doi.org/10.1016/j.scitotenv.2021.145471. approach towards plant health. J. King Saud. Univ. - Sci. 33, 101647 https://doi.
Jones, D.L., Freeman, C., Sánchez-Rodríguez, A.R., 2016. Waste water treatment. Encycl. org/10.1016/j.jksus.2021.101647.
Appl. Plant Sci. 3, 352–362. https://doi.org/10.1016/B978-0-12-394807-6.00019-8. Malmgren, A., Riley, G., 2018. Biomass Power Generation ☆, Reference Module in Earth
Jutakridsada, P., Saengprachatanarug, K., Kasemsiri, P., Hiziroglu, S., Kamwilaisak, K., Systems and Environmental Sciences. Elsevier Inc,. https://doi.org/10.1016/b978-
Chindaprasirt, P., 2019. Bioconversion of Saccharum officinarum leaves for ethanol 0-12-409548-9.11014-0.
production using separate hydrolysis and fermentation processes. Waste Biomass Mandal, S., Mallick, N., 2011. Waste utilization and biodiesel production by the green
Valoriz. 10, 817–825. https://doi.org/10.1007/s12649-017-0104-x. microalga Scenedesmus obliquus. Appl. Environ. Microbiol. 77, 374–377. https://
Kamath, R., Balachandra, M., Prabhu, S., 2020. Paddy crop and weed discrimination: a doi.org/10.1128/AEM.01205-10.
multiple classifier system approach. Int. J. Agron. 2020. https://doi.org/10.1155/ Miranda, A.F., Biswas, B., Ramkumar, N., Singh, R., Kumar, J., James, A., Roddick, F.,
2020/6474536. Lal, B., Subudhi, S., Bhaskar, T., Mouradov, A., 2016. Aquatic plant Azolla as the
Kandel, S., Malla, R., Adhikary, B.H., Vista, S.P., 2020. Effect of Azolla application on universal feedstock for biofuel production. Biotechnol. Biofuels 9, 221. https://doi.
rice production at mid-hills condition of Nepal. Trop. Agroecosyst. 1, 103–106. org/10.1186/s13068-016-0628-5.
https://doi.org/10.26480/taec.02.2020.103.106. Miranda, A.F., Liu, Z., Rochfort, S., Mouradov, A., 2018. Lipid production in aquatic
Kannan, D., Christraj, W., 2018a. Emission analysis of Azolla methyl ester with Bi2O3 plant Azolla at vegetative and reproductive stages and in response to abiotic stress.
nano additives for IC engine. Energy Sources, Part A Recover. Util. Environ. Eff. 40, Plant Physiol. Biochem. 124, 117–125. https://doi.org/10.1016/j.
1183–1189. https://doi.org/10.1080/15567036.2018.1474296. plaphy.2018.01.012.
Kannan, D., Christraj, W., 2018b. Emission analysis of Azolla methyl ester with BaO nano Miranda, A.F., Kumar, N.R., Spangenberg, G., Subudhi, S., Lal, B., Mouradov, A., 2020.
additives for IC engine. Energy Sources, Part A Recover. Util. Environ. Eff. 40, Aquatic plants, Landoltia punctata, and Azolla filiculoides as bio-converters of
1234–1241. https://doi.org/10.1080/15567036.2018.1476617. wastewater to biofuel. Plants 9, 1–18. https://doi.org/10.3390/plants9040437.
Karpanai Selvan, B., Das, S., Chandrasekar, M., Girija, R., John Vennison, S., Jaya, N., Mohamed, H.I., Abd-elsalam, K.A., 2021. Plant Growth-Promoting Microbes for
Saravanan, P., Rajasimman, M., Vasseghian, Y., Rajamohan, N., 2022. Utilization of Sustainable Biotic and Abiotic Stress Management. Springer. https://doi.org/
biodiesel blended fuel in a diesel engine – combustion engine performance and 10.1007/978-3-030-66587-6.

19
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

Mohammadi, M., Sedighi, M., Natarajan, R., Hassan, S.H.A., Ghasemi, M., 2021. Rai, A.N., Singh, A.K., Syiem, M.B., 2018. Plant Growth-Promoting Abilities in
Microbial fuel cell for oilfield produced water treatment and reuse: modelling and Cyanobacteria, Cyanobacteria: From Basic Science to Applications. Elsevier Inc.
process optimization. Korean J. Chem. Eng. 38, 72–80. https://doi.org/10.1007/ https://doi.org/10.1016/B978-0-12-814667-5.00023-4.
s11814-020-0674-3. Raimi, A., Roopnarain, A., Adeleke, R., 2021. Biofertilizer production in Africa: current
Mukhopadhyay, R., Sarkar, B., Jat, H.S., Sharma, P.C., Bolan, N.S., 2021. Soil salinity status, factors impeding adoption and strategies for success. Sci. Afr. 11, e00694
under climate change: challenges for sustainable agriculture and food security. https://doi.org/10.1016/j.sciaf.2021.e00694.
J. Environ. Manag. 280, 111736 https://doi.org/10.1016/j.jenvman.2020.111736. Rajendran, S., Priya, T.A.K., Khoo, K.S., Hoang, T.K.A., Ng, H.S., Munawaroh, H.S.H.,
Munyaka, S., Oki, P., Hattori, S., Tawaraya, K., 2020. Co-application of poultry-litter Karaman, C., Orooji, Y., Show, P.L., 2022. A critical review on various remediation
biochar with Azolla has synergistic effects on CH 4 and N 2 O emissions from rice approaches for heavy metal contaminants removal from contaminated soils.
paddy soils Heliyon Co-application of poultry-litter biochar with Azolla has Chemosphere 287, 132369. https://doi.org/10.1016/j.chemosphere.2021.132369.
synergistic effects on CH 4 and N 2 O emissions from rice paddy. Heliyon. https:// Rajeswari, S., Baskaran, D., Saravanan, P., Rajasimman, M., Rajamohan, N.,
doi.org/10.1016/j.heliyon.2020.e05042. Vasseghian, Y., 2022. Production of ethanol from biomass – recent research,
Muradov, N., Taha, M., Miranda, A.F., Kadali, K., Gujar, A., Rochfort, S., Stevenson, T., scientometric review and future perspectives. Fuel 317, 123448. https://doi.org/
Ball, A.S., Mouradov, A., 2014. Dual application of duckweed and azolla plants for 10.1016/J.FUEL.2022.123448.
wastewater treatment and renewable fuels and petrochemicals production. Razavipour, T., Moghaddam, S.S., Doaei, S., Noorhosseini, S.A., Damalas, C.A., 2018.
Biotechnol. Biofuels 7, 1–17. https://doi.org/10.1186/1754-6834-7-30. Azolla (Azolla filiculoides) compost improves grain yield of rice (Oryza sativa L.)
Naghipour, D., Ashrafi, S.D., Gholamzadeh, M., Taghavi, K., Naimi-Joubani, M., 2018. under different irrigation regimes. Agric. Water Manag. 209, 1–10. https://doi.org/
Phytoremediation of heavy metals (Ni, Cd, Pb) by Azolla filiculoides from aqueous 10.1016/j.agwat.2018.05.020.
solution: a dataset. Data Br. 21, 1409–1414. https://doi.org/10.1016/j. Roger, P.A., 1999. Use of blue-green algae and AzoZZa in rice culture.
dib.2018.10.111. Ruano, P., Delgado, L.L., Picco, S., Villegas, L., Tonelli, F., Merlo, M., Rigau, J., Diaz, D.,
Najar, I.A., Khan, A.B., 2010. Vermicomposting of invasive species azolla pinnata with Masuelli, M., 2016. We are IntechOpen, the world ’ s leading publisher of Open
eisenia fetida. Bioscan 5, 239–241. Access books Built by scientists, for scientists TOP 1%. IntechOpen, p. 13.
Narayanasamy, B., Jeyakumar, N., 2019. Performance and emission analysis of methyl Sabe, M., Pillinger, T., Kaiser, S., Chen, C., Taipale, H., Tanskanen, A., Tiihonen, J.,
ester of Azolla algae with TiO2 Nano additive for diesel engine. Energy Sources, Part Leucht, S., Correll, C.U., Solmi, M., 2022. Half a century of research on
A Recover. Util. Environ. Eff. 41, 1434–1445. https://doi.org/10.1080/ antipsychotics and schizophrenia: a scientometric study of hotspots, nodes, bursts,
15567036.2018.1548519. and trends. Neurosci. Biobehav. Rev. 136, 104608 https://doi.org/10.1016/j.
Nascimento, M.Do, Battaglia, M.E., Rizza, L.S., Ambrosio, R., Arruebarrena, A., neubiorev.2022.104608.
Palma, D., Curatti, L., 2019. Prospects of using biomass of N 2 - fi xing cyanobacteria Sadeghi, R., Zarkami, R., Sabetraftar, K., Van Damme, P., 2013. A review of some
as an organic fertilizer and soil conditioner. Algal Res. 43, 101652 https://doi.org/ ecological factors affecting the growth of Azolla spp. CJES Casp. J. Environ. Sci. 11,
10.1016/j.algal.2019.101652. 65–76.
Nosheen, S., Ajmal, I., Song, Y., 2021. Microbes as biofertilizers, a potential approach for Saha, B., et al., 2017. Biological Nitrogen Fixation for Sustainable Agriculture. In:
sustainable crop production. Sustainability 13, 1–20. https://doi.org/10.3390/ Meena, V., Mishra, P., Bisht, J., Pattanayak, A. (Eds.), Agriculturally Important
su13041868. Microbes for Sustainable Agriculture. Springer, Singapore. https://doi.org/10.1007/
Nurul Aina Nasriqah Binti, Ma’arof, Noor, Hindryawati, Siti Norhafiza Mohd, Khazaai, 978-981-10-5343-6_4.
Bhuyar, Prakash, Mohd Hasbi, Ab. Rahim, Gaanty Pragas, Maniam, 2021. Biodiesel Salehzadeh, A., Naeemi, A.S., Arasteh, A., 2014. Biodiesel production from Azolla
(Methyl Esters). Maejo Int. J. Energy Environ. Commun. 3, 30–43. https://doi.org/ filiculoides (Water Fern). Trop. J. Pharm. Res. 13, 957–960. https://doi.org/
10.54279/mijeec.v3i1.245153. 10.4314/tjpr.v13i6.19.
Ogunkunle, O., Ahmed, N.A., 2019. A review of global current scenario of biodiesel Sanyahumbi, D., Duncan, J.R., Zhao, M., Van Hille, R., 1998. Removal of lead from
adoption and combustion in vehicular diesel engines. Energy Rep. 5, 1560–1579. solution by the non-viable biomass of the water fern Azolla filiculoides. Biotechnol.
https://doi.org/10.1016/j.egyr.2019.10.028. Lett. 20, 745–747. https://doi.org/10.1023/A:1005386703592.
Ojuederie, O.B., Babalola, O.O., 2017. Microbial and plant-assisted bioremediation of Saravanan, P., Rajeswari, S., Kumar, J.A., Rajasimman, M., Rajamohan, N., 2022.
heavy metal polluted environments: a review. Int. J. Environ. Res. Public Health 14. Bibliometric analysis and recent trends on MXene research – a comprehensive
https://doi.org/10.3390/ijerph14121504. review. Chemosphere 286, 131873. https://doi.org/10.1016/j.
Oladoja, N.A., 2017. Appropriate technology for domestic wastewater management in chemosphere.2021.131873.
under-resourced regions of the world. Appl. Water Sci. 7, 3391–3406. https://doi. Selvi, A., Rajasekar, A., Theerthagiri, J., Ananthaselvam, A., Sathishkumar, K.,
org/10.1007/s13201-016-0495-z. Madhavan, J., Rahman, P.K.S.M., 2019. Integrated remediation processes toward
Paramasivam, P., Kanagesan, K., Bhuyar, P., Govindan, N., Mohd, M.H., Maniam, G.P., heavy metal removal/recovery from various environments – a review. Front.
2021. Biomass and lipid production from indigenous Nannochloropsis sp. by Environ. Sci. 7. https://doi.org/10.3389/fenvs.2019.00066.
employing stress factors for improved biodiesel production. Environ. Dev. Sustain. Shaji, H., Chandran, V., Mathew, L., 2021. Organic Fertilizers as A Route to Controlled
https://doi.org/10.1007/s10668-021-01910-2. Release of Nutrients, Controlled Release Fertilizers for Sustainable Agriculture.
Pawan, K.B., Singh, K., 2015. Response of nitrogen-fixing water fern Azolla Elsevier Inc,. https://doi.org/10.1016/b978-0-12-819555-0.00013-3.
biofertilization to rice crop. 3 Biotech 523–529. https://doi.org/10.1007/s13205- Shen, H.F.T., T.C, 1985. Culture o f azolla and rice plants growth and N2 fixation o f
014-0251-8. azolla plants growth and yield o f rice. Growth 22, 145–152.
Perera, F., 2018. Pollution from fossil-fuel combustion is the leading environmental Shin, S.E., Lim, J.M., Koh, H.G., Kim, E.K., Kang, N.K., Jeon, S., Kwon, S., Shin, W.S.,
threat to global pediatric health and equity: solutions exist. Int. J. Environ. Res. Lee, B., Hwangbo, K., Kim, J., Ye, S.H., Yun, J.Y., Seo, H., Oh, H.M., Kim, K.J.,
Public Health 15. https://doi.org/10.3390/ijerph15010016. Kim, J.S., Jeong, W.J., Chang, Y.K., Jeong, B.R., 2016. CRISPR/Cas9-induced
Peterson, C.A., Deiss, L., Gaudin, A.C.M., 2020. Commercial integrated crop-livestock knockout and knock-in mutations in Chlamydomonas reinhardtii. Sci. Rep. 6, 1–15.
systems achieve comparable crop yields to specialized production systems: a meta- https://doi.org/10.1038/srep27810.
analysis. PLOS One 15, 1–25. https://doi.org/10.1371/journal.pone.0231840. Singh, R.P., 2012. Organic fertilizers: Types, production and environmental impact,
Pirbazari, S.M., Norouzi, O., Kohansal, K., Tavasoli, A., 2019. Experimental studies on Organic Fertilizers: Types, Production and Environmental Impact.
high-quality bio-oil production via pyrolysis of Azolla by the use of a three metallic/ Sood, A., Uniyal, P.L., Prasanna, R., Ahluwalia, A.S., 2012. Phytoremediation potential of
modified pyrochar catalyst. Bioresour. Technol. 291, 121802 https://doi.org/ aquatic macrophyte, Azolla. Ambio 41, 122–137. https://doi.org/10.1007/s13280-
10.1016/j.biortech.2019.121802. 011-0159-z.
Piya, S., Shrestha, I., Gauchan, D., Lamichhane, J., 2018. Vermicomposting in organic Soudagar, M.E.M., Nik-Ghazali, N.N., Abul Kalam, M., Badruddin, I.A., Banapurmath, N.
Agriculture: Influence on the soil nutrients and plant growth. Int. J. Res 5, R., Akram, N., 2018. The effect of nano-additives in diesel-biodiesel fuel blends: a
1055–1063. comprehensive review on stability, engine performance and emission characteristics.
Prabakaran, S., Mohanraj, T., 2021. Optimization of biodiesel production from Azolla Energy Convers. Manag. 178, 146–177. https://doi.org/10.1016/j.
pinnata: investigation of CI engine characteristics using nano dosed biodiesel. enconman.2018.10.019.
J. Mech. Sci. Technol. 35, 1–9. https://doi.org/10.1007/s12206-021-0942-0. Subramaniam, M., Solomon, J.M., Nadanakumar, V., Anaimuthu, S., Sathyamurthy, R.,
Prabakaran, S., Mohanraj, T., Arumugam, A., 2021. Azolla pinnata methyl ester 2020. Experimental investigation on performance, combustion and emission
production and process optimization using a novel heterogeneous catalyst. Renew. characteristics of DI diesel engine using algae as a biodiesel. Energy Rep. 6,
Energy 180, 353–371. https://doi.org/10.1016/j.renene.2021.08.073. 1382–1392. https://doi.org/10.1016/j.egyr.2020.05.022.
Pradhan, B., Bhuyan, P.P., Patra, S., Nayak, R., Behera, P.K., Behera, C., Behera, A.K., Sudha, B., John, J., Meera, A.V., Sajeena, A., Jacob, D., Bindhu, J.S., 2021. Coconut
Ki, J.S., Jena, M., 2022. Beneficial effects of seaweeds and seaweed-derived bioactive based integrated farming: a climate-smart model for food security and economic
compounds: current evidence and future prospective. Biocatal. Agric. Biotechnol. 39, prosperity. J. Plant. Crop 49, 104–110. https://doi.org/10.25081/jpc.2021.v49.
102242 https://doi.org/10.1016/j.bcab.2021.102242. i2.7256.
Qiu, R., Hou, S., Meng, Z., 2021. Low carbon air transport development trends and policy Sundararaman, S., Kumar, P.S., Deivasigamani, P., Jagadeesan, A.K., Devaerakkam, M.,
implications based on a scientometrics-based data analysis system. Transp. Policy Al-Hashimi, A., Choi, D., 2021. Assessing the plant phytoremediation efficacy for
107, 1–10. https://doi.org/10.1016/j.tranpol.2021.04.013. Azolla filiculoides in the treatment of textile effluent and redemption of Congo red
Rabiu, S.D., Auta, M., Kovo, A.S., 2018. An upgraded bio-oil produced from sugarcane dye onto azolla biomass. Sustainability 13. https://doi.org/10.3390/su13179588.
bagasse via the use of HZSM-5 zeolite catalyst. Egypt. J. Pet. 27, 589–594. https:// Taghi Ganji, M., Khosravi, M., Rakhshaee, R., 2005. Biosorption of Pb, Cd, Cu and Zn
doi.org/10.1016/j.ejpe.2017.09.001. from the wastewater by treated Azolla filiculoides with H2O2/MgCl2. Int. J.
Rafiee, A., Khalilpour, K.R., 2018. Renewable Hybridization of Oil and Gas Supply Environ. Sci. Technol. 1, 265–271. https://doi.org/10.1007/bf03325841.
Chains, Polygeneration with Polystorage: For Chemical and Energy Hubs. Elsevier Talebi, M., Tabatabaei, B.E.S., Akbarzadeh, H., 2019. Hyperaccumulation of Cu, Zn, Ni,
Inc,. https://doi.org/10.1016/B978-0-12-813306-4.00011-2. and Cd in Azolla species inducing expression of methallothionein and phytochelatin

20
S. Prabakaran et al. Industrial Crops & Products 183 (2022) 114942

synthase genes. Chemosphere. https://doi.org/10.1016/j. Xu, H., Zhu, B., Liu, J., Li, D., Yang, Y., Zhang, K., 2017. Azolla planting reduces methane
chemosphere.2019.05.098. emission and nitrogen fertilizer application in double rice cropping system in
Tangahu, B.V., Sheikh Abdullah, S.R., Basri, H., Idris, M., Anuar, N., Mukhlisin, M., 2011. southern China. https://doi.org/10.1007/s13593-017-0440-z.
A review on heavy metals (As, Pb, and Hg) uptake by plants through Yadav, A.S., Kolluri, G., Gopi, M., Karthik, K., Malik, Y.S., Dhama, K., 2016. J. Exp. Biol.
phytoremediation. Int. J. Chem. Eng. 2011. https://doi.org/10.1155/2011/939161. Agric. Sci. 4, 368–383.
Tejada-Tovar, C., Villabona-Ortíz, A., Ortega-Toro, R., 2020. Determination of kinetic Yan, A., Wang, Y., Tan, S.N., Mohd Yusof, M.L., Ghosh, S., Chen, Z., 2020.
parameters in the biosorption of chromium (VI) in aqueous solution. Ing. Y. Cienc. Phytoremediation: a promising approach for revegetation of heavy metal-polluted
16, 129–143. https://doi.org/10.17230/ingciencia.16.31.6. land. Front. Plant Sci. 11, 1–15. https://doi.org/10.3389/fpls.2020.00359.
Temmink, R.J.M., Harpenslager, S.F., Smolders, A.J.P., Van Dijk, G., Peters, R.C.J.H., Yan, N., Marschner, P., Cao, W., Zuo, C., Qin, W., 2015. Influence of salinity and water
Lamers, L.P.M., Van Kempen, M.M.L., 2018. Azolla along a phosphorus gradient: content on soil microorganisms. Int. Soil Water Conserv. Res. 3, 316–323. https://
Biphasic growth response linked to diazotroph traits and phosphorus-induced iron doi.org/10.1016/j.iswcr.2015.11.003.
chlorosis. Sci. Rep. 8. https://doi.org/10.1038/s41598-018-22760-5. Yang, G., Ji, H., Sheng, J., Zhang, Y., Feng, Y., Guo, Z., Chen, L., 2020. Combining Azolla
Terry, L.M., Li, C., Chew, J.J., Aqsha, A., How, B.S., Loy, A.C.M., Chin, B.L.F., and urease inhibitor to reduce ammonia volatilization and increase nitrogen use
Khaerudini, D.S., Hameed, N., Guan, G., Sunarso, J., 2021. Bio-oil production from efficiency and grain yield of rice. Sci. Total Environ. 743, 140799 https://doi.org/
pyrolysis of oil palm biomass and the upgrading technologies: a review. Carbon 10.1016/j.scitotenv.2020.140799.
Resour. Convers. 4, 239–250. https://doi.org/10.1016/j.crcon.2021.10.002. Yao, Y., Zhang, M., Tian, Y., Zhao, Miao, Zeng, K., Zhang, B., Zhao, Meng, Yin, B., 2018.
Thiruvenkatachari, S., Saravanan, C.G., Edwin Geo, V., Vikneswaran, M., Azolla biofertilizer for improving low nitrogen use efficiency in an intensive rice
Udayakumar, R., Aloui, F., 2021. Experimental investigations on the production and cropping system. F. Crop. Res. 216, 158–164. https://doi.org/10.1016/j.
testing of azolla methyl esters from Azolla microphylla in a compression ignition fcr.2017.11.020.
engine. Fuel 287, 119448. https://doi.org/10.1016/j.fuel.2020.119448. York, N., Garden, B., 2016. Azolla: Botany, Physiology, and Use as a Green Manure
Umali, L.J., Duncan, J.R., Burgess, J.E., 2006. Performance of dead Azolla filiculoides Author ( s): Thomas A. Lumpkin and Donald L. Plucknett Published by: Springer on
biomass in biosorption of Au from wastewater. Biotechnol. Lett. 28, 45–50. https:// behalf of New York Botanical Garden Press Stable URL: 〈http://www.jstor.org/
doi.org/10.1007/s10529-005-9686-7. stable/4254158〉 Accessed: 25–06-2016 34, 111–153.
Watanabe, I., Roger, P.A., Ladha, J.K., Van Hove, C., 1992. Biofertilizer Germplasm Zhang, B., Ahmad, W., Ahmad, A., Aslam, F., Joyklad, P., 2022. A scientometric analysis
Collections at IRRI. approach to analyze the present research on recycled aggregate concrete. J. Build.
Whangchai, K., Souvannasouk, V., Bhuyar, P., Unpaprom, Y., 2021. Biomass generation Eng. 46, 103679 https://doi.org/10.1016/j.jobe.2021.103679.
and biodiesel production from macroalgae grown in the irrigation canal wastewater.
Water Sci. Technol. 84, 2695–2702. https://doi.org/10.2166/wst.2021.195.

21

You might also like