Journal of Cleaner Production 228 (2019) 1586e1599

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Journal of Cleaner Production

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

Review

Aquaponic trends and challenges e A review

Brandon Yep*, Youbin Zheng
School of Environmental Sciences, University of Guelph, Guelph, ON N1G 2W1, Canada

a r t i c l e i n f o a b s t r a c t

Article history: This article reviews current literature published on aquaponics, a growing technology which uses
Received 27 November 2018 aquaculture effluent to grow plants. Aquaponics offers a solution to several sustainability issues, such as,
Received in revised form limited water availability, environmental pollution, increasing fertilizer cost, and depletion of fertile soils.
11 April 2019
The commercial and scientific application of aquaponics is growing; however, there is yet to be a review
Accepted 22 April 2019
Available online 24 April 2019
which holistically analyses scientific literature to indicate what type of system performs optimally, what
will be the most dominant horticultural challenges as the commercial sector expands, and what direction
of aquaponic research will be most impacting. This review analyzed over 529 publications on aquaponics,
Keywords:
Aquaponics
from 1978 to 2018. Through a systematic process, 257 of the most constructive publications were further
Hydroponics analyzed and organized into varying groups based on content. The review found that in the past three 3
Sustainable agriculture years, over 160 scientific articles have been published on aquaponic technology, detailing numerous
Microflora trends, technological advancements and challenges associated with the system, consolidating the
Plant nutrition expansion of aquaponics and the need for a review. From publications investigating trends, it was found
Resource conservation that decoupled aquaponic systems are becoming increasingly popular over coupled aquaponic systems, a
deep water culture hydroponic component and media bed component are optimal for commercial and
research applications, respectively; Tilapia and dark leafy vegetables are the most successful species used
and Nitrospira may play a more important role in the aquaponic nitrification process than expected. From
publications investigating challenges, it was found that commercial aquaponics will face difficulty
growing high value flowering crops such as sweet peppers, tomatoes or cucumber, as a result of sub-
optimal nutrient ratios in aquaponic solution, specifically the reduced Kþ, Mgþ, and Caþ. Holistically, it
was found that the most important aspect of aquaponics that needs future research is the role plant
promoting microbes play in nutrient uptake. Considering plant growth promoting microbes are likely the
cause of aquaponic plants being able to achieve yields similar to that of hydroponics, despite nutrient
levels being significantly lower, future research in this field can be paramount to the beneficial use of
microbes in all plant production systems.
© 2019 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1587
2. Method . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1588
3. Results and discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1588
3.1. Trends . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1588
3.1.1. Aquaponic systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1588
3.1.2. Hydroponic components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1590
3.1.3. Fish species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1591
3.1.4. Plant species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1592
3.1.5. Nitrifying bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1592
3.1.6. Microflora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1593
3.1.7. Additional species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1593

* Corresponding author.
E-mail addresses: byep@uoguelph.ca (B. Yep), yzheng@uoguelph.ca (Y. Zheng).

https://doi.org/10.1016/j.jclepro.2019.04.290
0959-6526/© 2019 Elsevier Ltd. All rights reserved.
 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599 1587

3.2. Horticulture challenges . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1593

3.2.1. Nitrogen use efficiency . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1593
3.2.2. Nutrient limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1594
3.2.3. pH . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1595
3.2.4. Solids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1596
4. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1596
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1597
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1597

1. Introduction
Aquaponics is the process of growing aquatic organisms and
plants symbiotically, in which the effluent of aquaculture un-
dergoes microbial transformations to be used as a source of nutri-
ents for plant growth, while nutrient absorption from plants
remediates water for aquaculture. Others have systematically
defined aquaponics as ‘ … a production system of aquatic organ-
isms and plants where the majority (>50%) of nutrients sustaining
the optimal plant growth derives from waste originating from
feeding the aquatic organisms’ (Lennard, 2015; Palm et al., 2018).
The term “aquaponics” is a portmanteau of aquaculture and hy-
droponics. Aquaculture has been defined as “the farming of aquatic
organisms, including fish, molluscs, crustaceans and aquatic plant”
(Food and Agriculture Organization of the United Nations, 1988),
while hydroponics has been defined as “… the production of plants
in a soilless medium where by all of the nutrients supplied to the
crop are dissolved in water” (Diver, 2006). Although hydroponics is
considered a well-known technology, the term “aquaponics” is
relatively unfamiliar to the general public, as depicted in a Euro-
pean survey conducted by Mili
ci
c et al. (2017) in which over 50% of
individuals admitted they had not heard of aquaponics. Modern
day aquaponic systems have generally taken the form of recircu-
lating aquaculture systems (RAS). Within these systems, the waste
produced by aquatic organisms is filtered through tanks of natu-
rally occurring microbes, which break down organic compounds
and make them available for plant uptake. The main nutrient
conversion occurring is the transformation of ammonia (NHþ
nitrate (NO 3 ), via nitrifying bacteria. The aquaculture effluent,
loaded with nutrients, is then filtered into a hydroponic system
where plant roots and microbes are fertilized. The water is then
recycled back to the aquatic rearing tanks, remediated of cumulated
nutrients. This constructed closed-loop ecosystem has gained sig-
nificant attention in recent years, as it mitigates several concerns
developing in conventional agriculture.
Primarily, aquaponics has been perceived to have a high water
use efficiency, use a minimal amount of synthetic fertilizer, elimi-
nate the use of pesticides/herbicides or antibiotics, eliminate the
need for soil, simultaneously produce plant and fish, and minimize
the release of aquaculture waste into the environment. Although
there is a lack of quantifiable scientific data to back up some of
these merits, the concept of aquaponics alone has allowed it to be
regarded as one of the most sustainable forms of agriculture (Ko
et al., 2018; Palm et al., 2018). For example, the potential to increase
water efficiency in the agriculture industry is significant, consid-
ering that the industry consumes approximately 67% of available
freshwater (Shiklomanov, 1998), with areas such as the Middle East
and North Africa having their agriculture systems consume 90% of
the total fresh water available (FAO, 2005). Since most aquaponic
systems are some form of RAS, in which plants remove cumulating
nutrients for the fish, no water is lost, with the exception of fish
splashing, system evaporation, plant transpiration and necessary
water removals. RAS alone, use 90e99% less water than conven-
tional aquaculture systems, such as raceways or ponds (Timmons
and Ebling, 2010). Aquaponic systems further improves on RAS’
water use efficiency, as the water typically lost in waste filtration is
utilized by plants. Several studies have found that aquaponic sys-
tems typically use between 0.3 and 5.0% of total system water per
day (Maucieri et al., 2018; Rakocy et al., 2010). In comparison, some
basic recirculating hydroponic systems require complete nutrient
replacement every 2e3 weeks (Cooper, 1979; Resh, 1995). Aqua-
ponics also, by definition, utilizes at least 50% of nutrients initially
provided through fish feed as plant fertilizer, and therefore sup-
plements a substantially lower amount of fertilizer than hydro-
ponics and in some cases, supplements no fertilizer at all. Reducing
fertilizer use in agriculture has a substantial impact when consid-
ering that synthetic nitrogen fertilizer production has been esti-
mated to account for 57% of all agriculture energy demands
(Mudahar and Hignett, 1985) and phosphate reserves are predicted
to be half depleted in the next 60e70 years (Oelkers and Valsami-
Jones, 2008). Simultaneously, aquaculture systems only capture
25% of nitrogen in fish tissue, while 75% is excreted into the envi-
ronment (Hargreaves, 1998; Krom et al., 1995). Aquaculture oper-
ations require a filter system to remove toxic compounds such as
ammonia, nitrite, and suspended particles from the system. These
compounds, if not properly managed, may leach into neighbouring
environments and cause water eutrophication. Considering aqua-
culture is the fastest growing agriculture industry in the world and
is predicted to provide 54% of the estimated 200 million tons of fish
3 ) to demanded by 2030, this is a sector which can have an immense
impact on the environment (Food and Agriculture Organization of
the United Nations, 2018). Finally, given that aquaponics uses a
hydroponic component and therefore does not require soil; its use
can be optimized in controlled environments in urban areas. This
can help mitigate production loss from the land shortage caused by
urbanisation.
Aquaponic systems have the potential to avoid some of the
major resource inefficiencies present in conventional agriculture;
however, achieving the resource efficiency as mentioned above, has
been largely unquantified in scientific publications. Based on
several past reviews, successful aquaponic operations must
consider the impacts of system design (Palm et al., 2018), system
water pH control (Tyson et al., 2011), aeration and filtration tech-
nologies (Danaher et al., 2013), acceptable nutrient ranges (Delaide
€ nig et al., 2016), pairing of plant and fish species, microbial populations,
nitrogen levels, quantity and type of feed (Endut et al., 2010), pest
management and effective marketing. These factors are the main
concern of those managing the system. In a broader sense, aqua-
ponics is an even more complex system which involves multiple
disciplines, such as aquaculture, microbiology, ecology, horticul-
ture, agriculture, chemistry and engineering. As a result, complete
and comprehensive reviews on aquaponics are difficult. There are a
few literature reviews already available on aquaponics; however,
each of these reviews generally focuses on a single concept of
1588 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
aquaponics, such as management practices (Tyson et al., 2011),
socio-economic feasibility (Junge et al., 2017), hydroponic systems
(Pattillo, 2017), system design (Palm et al., 2018) and industry
trends (Ko € nig et al., 2018). The most comprehensive and recent of
these reviews was arguably the review by Goddek et al. (2015).
Since this review, there has been over 160 scientific publications on
aquaponics. These publications have cultivated technological ad-
vancements, comprehensive industry surveys, horticulture chal-
lenges, and suggestions for future research. Specifically, there has
been several publications focussed on new system designs, evalu-
ation of hydroponic components, successful plant and fish species,
the role of plant growth promoting microbes and the challenges of
using the system from a horticultural perspective. These topics
have yet to be holistically summarized in a literature review.
Therefore, this review will summarize current trends in these
topics, as well as provide critical insight on their value to both the
commercial and research sectors.
Through the aforementioned topics, this review aims to sum-
marize the following: 1. the most successful system factors based
on current trends in the aquaponic industry, 2. the most limiting
challenges of the aquaponic industry from a horticulture stand
point, and 3. the most impacting research directions for the aqua-
ponic industry.
2. Method
This review was developed using a systematic, strategic and
comprehensive literature review on peer reviewed aquaponic
publications. This was achieved by analysing every publication
retrieved with the keyword ‘aquaponic’ from the oldest publica-
tions available (1975) to the newest (2018) on both the web of
science (213 publications, see Fig. 1.), and the University of Guelph
online library, via Primo (529 publications). Based on the results of
this search, publications with significant value were collected in the
reference software Mendeley (255 publications). Publications were
considered of significant value if they had the three following at-
tributes: peer reviewed, contain material relating to current trends
and challenges of aquaponics, and used creditable scientific
methods. Publications were then categorized into the following
three categories: trends, horticulture challenges, and advance-
ments. Trends was further divided into the following sections:
system design, hydroponic component, plant species, fish species,
Fig. 1. Web of science citation report for search term ‘aquaponic’.
and microflora. Horticultural challenges were divided into nitrogen
use efficiency, nutrients, system water pH and solids. Advance-
ments were later incorporated into either folder based on an
overlap of content. Furthermore, key publications referenced in the
literature, which were not previously collected due to limited ter-
minology of ‘aquaponic’, were additionally collected in the Men-
deley software, expanding the breadth of aquaponic literature
reviewed. From this literature review, it became evident that
aquaponic publications have been released at an exponential rate in
the past 3 years (over 160 publications), illustrating the importance
of a literature review on the subject.
3. Results and discussion
3.1. Trends
After conducting the literature review, it became apparent that
there were major trends in the following: types of aquaponic sys-
tems, hydroponic components, plant species, fish species, nitrifying
bacteria, microflora and additional species. Each sequential section
describes the specific trends for each category, as well as a dis-
cussion on their associated impact on both the commercial and
research sectors.
3.1.1. Aquaponic systems
With the hydroponic component not taken into consideration
(as several different styles can be used), modern commercial
aquaponic systems can be divided into coupled aquaponic systems
(CAS), and decoupled aquaponic systems (DAS) (Forchino et al.,
2017). CAS consist of one continuous system loop, in which the
water has only one direction or outlet in each tank. An example of a
classic CAS would be the UVI (University of the Virgin Islands)
aquaponic system or the Integrated Aqua-Vegeculture System,
illustrated in Fig. 2. The majority of modern aquaponic research
articles use varying CAS (Ru et al., 2017; Gullian Klanian et al., 2018).
Most scientific articles are focussed on a certain aspect of aqua-
ponics, as opposed to the system design, and as a result most CAS
used are no more sophisticated than the modern UVI system. In
comparison, DAS utilizes sub-loops within the system in which
water can travel in more than one direction in some tanks, shown
in Fig. 3. This is done primarily for superior filtration, and increased
ability to manipulate nutrient concentrations and system water pH
 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
~ Direction of System Water
Aquaculture
Tank
Filter
Clarifier
Tank
Aquaculture
Tank
Sump Tank
(Pump)
Fig. 2. Example of coupled aquaponic system. Design modified from the University of the Virgin Islands Commercial Raft System(Rakocy, 2012) and designs presented by (Palm
et al., 2018) and Goddek et al., (2016).
~ Direction of System Water
Aquaculture
Tank
Clarifier
Filter
Tank
Aquaculture
Tank
Sump Tank
(Pump)
Fig. 3. Example of decoupled aquaponic system. Design modified from decoupled designs presented by Kloas et al. (2015) and the University of the Virgin Islands Commercial Raft
System (Rakocy, 2012).
(Goddek and Keesman, 2018). The first example of DAS was the
system put forth by Naegel (1977); however, it was not until 2015
that the first modern day DAS was described by Kloas et al. (2015).
The first record of a modern DAS was published in 2015 by the
Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Berlin
Germany (Kloas et al., 2015). The system was termed Aquaponic
System for emission-free Tomato and Fish Production and was
unique in that it had two separate loops that solution could flow
between in the system. One loop was a filtration loop, which
allowed water to be mechanically filtered and continuously
returned to the fish tanks without encountering the plants. The
second loop (only accessible after going through the first loop)
circulated water between the hydroponic component and a tank
where fertilizer could be added. This allowed water parameters to
be changed more drastically for the hydroponic portion without
affecting the aquaculture portion of the system. Plants prefer a
hydroponic root zone pH of 5.8e6.2, whereas most aquatic or-
ganisms prefer a pH of 6.5e9 (Rakocy, 2003; Timmons and Ebling,
2010). This system allowed pH changes and fertilizer additions to
occur without directly affecting the solution in the fish tanks. After
the introduction of this system, DAS began to gain considerable
interest. Schmautz et al. (2016) report modifying their CAS system
to a DAS, while also adding a number of hydroponic components to
their system. The advantage to using numerous hydroponic com-
ponents is the increased stability in water quality and the ability to
grow and compare a variety of crops. Goddek and Keesman (2018)
reported that there are now numerous modern DAS in Europe
(Tilamur, IGB, and Inagro facilities), some of which have 3500 m2 of
grow space (NerBreen, Spain). Although it seems aquaponic
1589
Degassing Hydroponic
Bioreactor Tank System
Nutrient and pH
Adjustment Tank
(Pump)
Two Way
Bioreactor Degassing
Tank
Hydroponic
System
systems are moving towards DAS, at least in Europe, there are some
disadvantages to the system in comparison to CAS. The most pre-
dominant challenge to DAS is the increased initial cost to construct.
There are no reports currently available on the economics of DAS
versus CAS, understandably so, considering how recent DAS are.
However, it is presumed to have higher initial costs, as a result of
increased pumps, pipes and tanks. Furthermore, DAS require more
space than CAS, which takes away valuable space for growing
plants. Considering that only 31% of aquaponic facilities are
currently predicted to be profitable and 47% of commercial aqua-
ponics facilities rely on other agricultural product/service for in-
come, adding more costs to the system would be a challenge to the
commercial sector (Love et al., 2014). A study carried out by
Tokunaga et al. (2015) found that a mid-sized aquaponic farm
would have an initial investment cost of $217,078 USD. In this
scenario a mid-sized aquaponic farm would consists of a fish tank
volume of 76 m3 and a plant growth bed of 1142 m2. The study
found that the largest portion of expenses in the fish system were
the cost of tanks and pumps. Engle (2015) similarly found that
aquaponic infrastructure costs were between $285,134 and
$1,030,536, for small and large UVI systems respectively. DAS also
require additional fertilizer to be added to the hydroponic loop, as it
is separated to a higher degree from the filtration/mineralization
tanks, which supports much of the nutrient reserves, therefore
adding another cost to the system (Goddek and Keesman, 2018). To
overcome some of these disadvantages, novel aquaponic design
concepts are beginning to emerge. Goddek and Keesman (2018) put
forth the idea of incorporating a reverse osmosis filter (desalination
unit) within an aquaponic system to remove salts and concentrate
1590 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
nutrients into water that can be directly added to a hydroponic loop
in DAS. Such a system would allow cleaner water for the fish, while
also concentrating nutrients to be used in a more effective manner,
mitigating the costs of additional fertilizer. However, this system
would require a high quantity of energy to run and would only be
economical on a large scale, considering the high costs of such a
filtration unit. Less extreme options to improve filtration methods
have also been suggested. Within both DAS and CAS, modification
to the filtration units within these systems has also been investi-
gated in order to improve management and mitigate solid particles
entering the hydroponic component. Danaher et al. (2013) inves-
tigated the use of a swirl separator in place of a clarifier in attempt
to concentrate solids in the clarifier to the bottom and to also in-
crease the flow of water leaving the clarifier. Their study found no
difference in fish and plant yields or system water quality (pH, DO,
etc.) from using the swirl separator in comparison to a clarifier;
however, they found that the swirl separator was simple to install,
required minimal labour and decreased settling time for particulate
matter. Future improvements to filters will be an important
consideration, given that increased filtration has been found to
increase plant yields and fish health (Sikawa and Yakupitiyage,
2010). As aquaponics expands into the commercial sector, entities
may quickly adapt DAS over CAS. Entities should be cautioned that
it is unclear if DAS are as sustainable and economical as CAS, based
on their higher requirement for space, infrastructure and additional
fertilizer. Entities should investigate both system designs based on
their needs, before implementing either, and future research
should be allocated to contrasting the profitability and sustain-
ability of DAS to CAS, to clarify their advantages and disadvantages
to aquaponic growers. With aquaponics primary selling point of
being a sustainable system, developing commercial systems which
are truly sustainable is of utmost value. To add to the complexity of
aquaponic systems, either CAS or DAS may use varying hydroponic
systems, further affecting the productivity and efficiency of the
system.
3.1.2. Hydroponic components
The three most common hydroponic systems used in aqua-
ponics are varying forms of: i) deep water culture (DWC) or floating
raft technique, ii) media filled grow beds, or iii) nutrient film
technique (NFT) (Goddek et al., 2015; Maucieri et al., 2018). A re-
view on hydroponic systems in aquaponic publications found that
43% used a media-based system, 33% used DWC, 15% used NFT, and
9% used other less common hydroponic systems (Maucieri et al.,
2018). Less common hydroponic systems include: drip irrigation
(Schmautz et al., 2016), ebb and flow (Knaus and Palm, 2017), and
vertical towers/walls (Khandaker and Kotzen, 2018). The review
has found that hydroponic components should be evaluated
differently in aquaponic systems than conventional hydroponic
systems. In aquaponics, hydroponic components must handle so-
lution which is higher in total suspended solids (Monsees et al.,
2017b; Rakocy et al., 2004), and is also dependent on beneficial
microbes in enhancing plant nutrient uptake (Bartelme et al., 2018).
Several scientific articles have compared some of the above hy-
droponic systems against one another in aquaponic systems;
however, their results typically vary from study to study. This
variability is likely due to differences in: aquaponic/filtration sys-
tems, environmental conditions and practical experience in
running an aquaponic system.
3.1.2.1. Nutrient film technique. A study by Lennard and Leonard
(2006) investigating the effectiveness of a NFT system compared
to a media culture and DWC system, found that the NFT system had
the lowest yields of lettuce and consequently removed the least
amount of nitrate (20% less efficient at nitrate removal). This may
be attributed to a lower percent of roots in contact with the
aquaponic water, as opposed to DWC in which all of the roots are
completely submerged in the water. The root mats which occur in
NFT systems cause roots to fold on top of each other due to the
limited space provided in the trough (Cooper, 1979). This may limit
root contact with the nutrient water. This conclusion was sup-
ported in the recent review by Maucieri et al. (2018), who reviewed
122 articles and found that NFT was the least successful hydroponic
component in aquaponic systems. They found that NFT systems, on
average, had lower yields and were less popular in research articles
than media culture and DWC systems. Additionally, NFT has limited
surface area for beneficial microbes, and as a result a biofilter is
necessary (Maucieri et al., 2018). Despite these drawbacks, NFT is
still widely used in commercial systems, due to its low initial costs,
simple design and overall ease of operation (Goda et al., 2015;
Lennard and Leonard, 2006). Future studies should investigate
the effectiveness of NFT against DWC and media grow beds in larger
commercial aquaponic settings as opposed to small scale research
systems.
3.1.2.2. Media culture. Media culture is the use of inert solids (i.e.
hydroton, perlite, cocopeat) in grow beds, to grow plants. Media
culture is the most common hydroponic system used in aquaponic
research publications, as it can be used for a variety of plant species
and is a feasible option for small scale research systems (Maucieri
et al., 2018; Schmautz et al., 2016). Media beds also provide more
stability for root growth, and as a result larger plants may be better
adapted to such systems (Molovan and Ba la, 2015). Another benefit
of media based hydroponics, is that the substrates provide enough
surface material for nitrifying bacterial growth, and physical
filtration, so that a biofilter is not needed (Maucieri et al., 2018).
Conversely, often times the substrates closest to the initial inflow of
water become clogged with sediment and create an uneven ferti-
gation for the rest of the hydroponic grow space or even create
anaerobic zones (Mcmurtry et al., 1997; Rakocy, 2003). This can be
overcome by flushing the system with filtered water, or by manu-
ally removing, cleaning and replacing the grow bed medium
(Pattillo, 2017); however, this is an additional maintenance opera-
tion which can increase the cost of production. For these reasons,
scaling up systems which use media culture can be difficult to
maintain. Media culture should be recognized as a more suitable
hydroponic component for smaller scale aquaponic operations,
while hydroponics components with minimal maintenance needs,
such as DWC, should be recognized for more large scale operations
(Palm et al., 2018).
3.1.2.3. Deep water culture. DWC, also referred to as deep water
technique, or floating raft culture (Pattillo, 2017), has been defined
by Vermeulen and Kamstra (2013) as “systems with a water level
generally more than 5 cm deep, with the water kept in circulation,
while plants float on the water in Styrofoam plates or otherwise
held in position for the crop production”. The use of floating rafts is
the most common commercial hydroponic component according to
an international study by Love et al. (2015a). DWC is popular
amongst commercial growers because of their low maintenance,
maximized root to water contact and ability to support a large
number of plants with minimal materials (Molovan and Ba la, 2015;
Pattillo, 2017). Lennard and Leonard (2006) found that DWC
removed the most nitrate from an aquaponic system compared to
NFT and media culture. Another advantage to DWC is that in the
event of a power outage, plants may survive for up to two weeks
without water flow, whereas a prolonged power outage in NFT or
media-culture would be fatal for plants (Rakocy, 2003). In a study
by Forchino et al. (2017), it was determined that DWC had a lower
environmental impact than media-culture systems, with the
 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
primary difference being attributed to the inert material required
for the grow beds in media culture. Although this system requires
more water than media culture or NFT, many publications have
recorded improved water use efficiency in DWC systems. Love et al.
(2015b) found that a DWC system used 1% of its total system water
per day. No other hydroponic component has been reported to have
such a high water use efficiency, which is significant considering
generalized aquaponics systems are widely promoted for water use
efficiencies equivalent to DWC. The biggest challenge in using DWC
is the requirement to aerate (incorporate oxygen) into the water in
the grow beds. Since aquaponic systems depend on a high level of
aerobic microbes for nutrient uptake and plant roots require oxy-
gen to uptake nutrients, there is a very high biological oxygen de-
mand in the grow beds (Pattillo, 2017). Silva et al. (2018) developed
a novel hydroponic system in which plants were half submerged in
DWC while the other half of roots was exposed to air in between the
water and the suspened raft. This system was termed Dynamic Root
Floating Technique. In comparison to standard DWC, their system
reduced energy costs by 10.3% in a small scale system, which
equated to an 11% cheaper total electrical cost for the full growth
cycle of Brassica rapa sub-species chinensis (pak choi) (32 days).
Furthermore, this study found no difference in dissolved oxygen
and total ammonia nitrogen (TAN) in the fish tanks, or differences
in either plant or fish growth parameters, which were the primary
concerns when removing forced air from an aquaponic system. A
disadvantage of DWC is the increased presence of pests. Rakocy
(2003) have cautioned that DWC systems may harbour
zooplankton, ostracods, snails and other aquatic pests which may
slow plant growth by eating root hairs and beneficial microbes.
3.1.2.4. Vertical towers/walls, ebb and flow, drip irrigation. The less
frequently (9%) reported hydroponic components used in aqua-
ponic systems are primarily Ebb and Flow or flood and drain tables,
drip irrigation and vertical towers/walls. Although less common in
aquaponic publications, these systems can be effective under
certain circumstances. Schmautz et al. (2016) found that tomato
plants under drip irrigation had the highest yield (18.7 kg/m2) in
comparison to NFT (17.5 kg/m2) and DWC (17.4 kg/m2). A downside
to drip irrigation is that it requires a significantly higher amount of
energy than DWC or NFT (Schmautz et al., 2016). Another potential
challenge of using drip irrigation with aquaponics is the buildup of
solid particles in the drip lines. Palm et al. (2014) was the only study
to report the successful use of a formal Ebb and Flow in aquaponic
publications. Advantages of ebb and flow include increased aera-
tion with less energy use, increased flexibility in periods of aridity
and saturation, minimal infrastructure and increased surface area
for microbial growth (Palm et al., 2014; Pattillo, 2017). A challenge
to these systems would be providing filtered water to the fish tanks
at a constant rate, given the variable rates in flooding the tables.
However, the merit to these advantages and disadvantages remains
unclear due to limited published research. The most recent hy-
droponic system development for aquaponic systems is vertical
towers or walls. The potential for aquaponics to be a form of urban
agriculture has led to the development of systems with a vertical
hydroponic component. At Greenwhich Aquaponics Lab in the UK,
Khandaker and Kotzen (2018) investigated the potential of using a
hydroponic tower in an aquaponic system, as well as potential
substrates to be used in the towers. Vertical hydroponics can also be
extended to having multiple layers of NFT, DWC, or drip irrigation
as described by Pattillo (2017). Pattillo (2017) also cautions, how-
ever, that vertical systems, specifically towers, are susceptible to
biofouling and clogging.
Based on several articles comparing hydroponic components in
aquaponics, the following conclusions can be made: 1) natural
variations, management techniques, and application of hydroponic
1591
components in aquaponic systems make it difficult to derive con-
clusions on which component is optimal; 2) hydroponic compo-
nents must be evaluated differently for aquaponic systems to
account for higher suspended solids and the dependence of mi-
crobes; 3) media beds are ideal for small scale and research aqua-
ponic systems, based on its ability to grow a variety of plants and
mitigate the use of a biofilter; 4) the DWC component appears to be
optimal for commercial applications, based on its low environ-
mental impact, maximized root to water contact, consistent record
of achieving high yields and ability to match water use efficiencies
for which aquaponics is regarded for.
3.1.3. Fish species
An international survey conducted by Love et al. (2014) found
that out of 257 aquaponic respondents, 69% used Oreochromis
niloticus (tilapia), 43% used ornamental fish and 25% used Silur-
iformes (catfish) in their commercial operations. Other commonly
reported species of fish used in commercial aquaponics include:
Oncorhynchus mykiss (Rainbow trout), Cyprinus carpio (Common
carp), Lates calcarifer (Barramundi), Micropterus salmoides (Large-
mouth bass), Piaractus mesopotamicus (Pacu), Pomoxis (crappies)
and Maccullochella peelii (Murray cod) (Rakocy et al., 2006). Other
species of aquatic organisms (i.e. Acipenseridae (Sturgeon), Salveli-
nus alpinus (Artic charr)) have been suggested to work well in
aquaponic systems but have not been reported in scientific publi-
cations. The primary characteristic for an aquatic organism to be
productive in aquaponics is the ability to tolerate high population
densities and high levels of total suspended solids, nitrogen,
phosphorous and potassium (Rakocy et al., 2006; Timmons and
Ebling, 2010). Generally, fish should not be stocked higher than
0.06 kg/L, although species which can thrive close to this density
level are ideal for aquaponics (Rakocy et al., 2006). The most
commonly used, and arguably most successful fish species used in
aquaponics is Nile tilapia, followed by Carp and African Catfish. In
the literature review conducted here, 43% of published articles used
a tilapia species as the primary aquatic organism. Tilapia thrive in
aquaponic systems primarily because they are tolerant to un-
optimal water conditions. El-Sayed (2006) classified tilapia to be
fast growing, able to withstand stress and disease, tolerant to a
wide range of environmental conditions, and able to feed on low
trophic levels. Tilapia are naturally low trophic omnivores and are
microphagus, meaning they consume small organisms such as
phytoplankton as well as small organic particles (El-Sayed, 2006).
As a result, tilapia can tolerate higher total suspended solids, and
nitrite levels up to 44.67 mg/L, which are normally limiting factors
for other aquatic species (Ru et al., 2017). Additionally, Tilapia do
not require a high quantity of growing space on account of their low
dissolved oxygen requirement (can survive at 0.5e1.0 mg/L of dis-
solved oxygen) and can therefore be stocked at a higher rate, which
is ideal for reaching the nutrient demands of plants in aquaponics
(El-Sayed, 2006). Based on aquaponic articles currently available, it
is not clear if excretion from different species have a significant
affect on the nutrient levels in aquaponic solution or plant yield. For
example, African catfish, Nile tilapia and Common carp all pro-
duced water effluent with nitrate between 20 and 42.9 mg/L and
phosphorous between 8.2 and 17 mg/L (Endut et al., 2010; Rakocy
et al., 2004; Roosta, 2014). Concurrently, Knaus and Palm (2017)
found that the use of Common carp effluent resulted in higher
yields of cucumber over tilapia effluent, while tilapia effluent
resulted in higher yields of tomatoes. Although it is not clear why
tomatoes grew better with tilapia effluent over carp effluent, it was
noted that tilapia had a higher metabolic feeding activity than carp.
This may indicate that tilapia were releasing more feces (nutrients)
into the water than carp. The authors also suggested that using
multiple species may be advantageous for developing a more
1592 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
complete nutrient water profile in the water. The use of multiple
aquatic species (polyculture) in aquaponics to develop improved
solution for plant growth has not been investigated and carries
great research potential, considering the limitation in nutrients for
some plants in aquaponic solution, as is discussed later. In terms of
economic contribution, aquaculture product provides minimal
value (Bailey and Ferrarezi, 2017; Engle, 2015), with some aqua-
ponic studies finding plants provided 3.6 fold the revenue than
aquaculture (Rakocy et al., 2004). Bosma et al. (2017) found that it
would be difficult to run a profitable aquaponic operation in the
Philippines with a low value fish such as catfish. They emphasized
that the main source of income would come from the plants, and
that only high value fish such as Scortum barcoo (Jade Perch) would
contribute a significant amount to the income of an aquaponic
farm; however, high value fish typically require increased water
quality (increased space, lower acceptable suspended solids) which
does not complement most aquaponic systems.
3.1.4. Plant species
In general, leafy vegetables have been the preferred crop to
grow in aquaponic systems, as they grow well in nitrogen
concentrated water, have a short growing period, do not have high
nutrient requirements and there is generally a high demand for
them globally (Bailey and Ferrarezi, 2017). Although flowering
crops have a higher economic value than leafy vegetables, they are
more difficult to grow in aquaponic systems due to their heavy
nutrient requirements of phosphorous and potassium, their
increased susceptibility to pests and diseases, and their longer
growing cycles (Rakocy, 2003). Bailey and Ferrarezi (2017) found
that the UVI system (214 m2 grow space) could make $110,000 a
year selling only Ocimum basilicum (basil), whereas they would
only make $6400 selling Abelmoschus esculentus (okra). The same
study also indicates that the value of the crop does not necessarily
correlate with profit. In their study they found that although basil
had the highest value per kg ($8.80e11.03 USD), Bibb (Boston)
lettuce produced more income per week per m2 ($7.50e9.20 USD)
compared to basil ($3.96e4.96 USD), because of increased yield and
increased planting density. All fruiting crops (i.e. cantaloupe,
zucchini, and cucumber) did not have weekly incomes per m2
above $1.32 USD. Similarly, most aquaponic economical studies,
which found the system to be profitable, were using leafy vegeta-
bles. Rupasinghe and Kennedy (2010) found an aquaponics farm
growing lettuce and barramundi, had a $22,800 higher annual
economic return than the two standalone systems (Rupasinghe and
Kennedy, 2010). The aquaponic farm saved $1320 on nitrogen and
phosphorus fertilizer, $1269 on effluent disposal and $3391 on total
variable costs, over the period of a year (Rupasinghe and Kennedy,
2010). Similarly Adler et al. (2000) estimated that combining a trout
farm producing 22,680 kg per year, with a NFT system growing
lettuce and basil, would result in return of 12.5%, and increased
profit through decreased costs of water remediation and increased
revenue from plant production (67% of revenue). This may explain
why commercial aquaponic growers primarily produce leafy greens
and herbs in their systems. Love et al. (2015a) found that com-
mercial aquaponic growers most commonly grew basil (81%), salad
greens (76%), non-basil herbs (73%), Solanum lycopersicum (to-
matoes) (68%), Lactuca sativa (head lettuce) (68%), Brassica oleracea
(kale) (56%), Beta vulgaris subspecies cicla (chard) (55%), pak choi
(51%), Capsicum annuum (pepper) (48%), and Cucumis sativus (cu-
cumbers) (45%). Furthermore, aquaponic systems have expanded to
grow plants which can thrive in salt water. An important plant
species that can be grown in salt or brackish water aquaponics is
Salicornia persica (Kong and Zheng, 2014; Turcios and Papenbrock,
2014). Salicornia is a halophyte tolerant of high salinity and able to
absorb high levels of nitrate and phosphate. Furthermore, Salicornia
shoots are a nutritious vegetable high in lipids, omega-3s, and
minerals, which are gaining popularity in the European market
(Turcios and Papenbrock, 2014). As aquaponics advanced over the
years, so has the number of successful of plant species; however,
minimal scientific articles have cited the use of aquaponics to grow
flowering plants. Future studies should investigate the effective-
ness of aquaponics for the floriculture industry.
3.1.5. Nitrifying bacteria
Arguably one of the most important organisms in any aquaponic
system is the nitrifying bacteria. Nitrifying bacteria primarily con-
verts TAN into nitrate (NO 3 ), a form of nitrogen plants can readily
uptake (Canfield et al., 2010). This nitrogen conversion occurs in a
two-step bacterial process. Before the bacterial process, TAN must
first be made available in the water. TAN may be excreted by fish in
the form of urine (urea) and feces, of which nitrogen makes up
between 10 and 40% of, or released through gills as ammonia
(Wongkiew et al., 2017a). Once in the water, TAN can be utilized as
an energy source for ammonia oxidizing bacteria, while NHþ 4 itself
can be taken up by plants. Ammonia oxidizing bacteria produce
nitrite, which is simultaneously used as an energy source for nitrite
oxidizing bacteria, where it is converted into nitrate. Nitrifying
bacteria may grow throughout the system, but are typically more
concentrated in biofilters, if present. Nitrification is optimal when
the temperature is between 25 and 30  C, the pH is between 7 and 9
(optimally 7.8 according to Antoniou et al. (1990)), and oxygen is
below 20 mg/L (Rakocy et al., 2006). Nitrite at high levels
(0.25e1 mg/L) (Jiang et al., 2014) can enter the blood stream of
aquatic organisms and oxidize the iron in hemoglobin molecules,
changing it from the ferrous state to the ferric state (Timmons and
Ebling, 2010). This creates methemoglobin, a toxic compound
which can turn the blood brown and result in the lethal Brown-
Blood Disease. Nitrate, however, is a generally non-toxic com-
pound which can be found at levels exceeding 1000 mg/L in
freshwater environments without negative effects on aquatic life
(Timmons and Ebling, 2010). In aquaponic systems, nitrate has been
reported to be harmless at concentrations of 150e300 mg/L (Graber
and Junge, 2009; Hu et al., 2015). Goddek et al. (2015) summarized
that based on previous studies, the three major nitrifying bacteria
in aquaponic systems are Nitrobacter, Nitrosomonas, and Nitrospira.
However, the notion that Nitrosomonas is the primary nitrite
oxidizing bacteria and Nitrobacter is the primary ammonia
oxidizing bacteria, is quickly changing. A study released by
Schmautz et al. (2017) investigating microbial communities in
varying locations of an aquaponic system, found that Nitrospira
made up 3.9% of the microbial community in the biofilter, while
Nitrobacter and Nitrosomonadales only made up 0.11% and 0.64%
respectively. Similarly, Bartelme et al. (2017) found that in the
biofilter of a RAS, Nitrospira amoA was the most populated nitrifying
bacteria, while Nitrobacter populations were not detected. They
also found that Nitrospira amoA populations remained stable over
time despite competing species (ammonia-oxidizing archea),
indicating a stable co-existence between microbes. This was a
significant discovery considering that Nitrospira is believed to
include some strains which can convert ammonia to nitrate in a
one-step process (Daims et al., 2015). It is known that complete
nitrification (i.e., NHþ 
3 to NO3 ) in a one step process, is an ener-
getically more favourable reaction than the two nitrification steps
carried out by ammonia oxidizing bacteria and nitrite oxidizing
bacteria. However, previous studies have found the phenomenon of
nitrification only occurring in the less favourable two step-process.
This mindset has changed recently, as Daims et al. (2015) has found
that a strain of Nitrospira, Candidatus Nitrospira inopinata, is a
‘comamox’ (complete ammonia oxidizer). Furthermore, they found
this strain able to thrive in the following areas: biofilms, flocs and
 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
microcolonies of low substrate concentrations (Daims et al., 2015).
It has also been found that Nitrospira are more prevelant over
Nitrobacter in environments with lower nitrite and ammonium
concentrations, due to a lower half-saturation constant (Ks)
(Blackburne et al., 2007). This may indicate that Nitrospira will have
higher populations in aquaponic systems which have an efficient
nitrifcation process, as such environments should have low nitrite
levels and high nitrate levels. Future studies should investigate the
varying strains of Nitrospira in aquaponic biofilters, and determine
the effects of nitrogen use efficiency when such strains are present.
Furthermore, within these biofilters, nitrifying bacteria often form
biofilms or relationships with heterotrophic organisms, such as
protozoa, micrometazoa and heterotrophic bacteria (Timmons and
Ebling, 2010). These organisms may play a role in enhancing
nutrient availability to plants.
3.1.6. Microflora
Bartelme et al. (2018) outlined that plant growth promoting
microorganisms (PGPM) or microflora may play a major role in the
plant's ability to uptake nutrients in an aquaponic system. Although
many studies have investigated PGPM in soil environments, there
are minimal studies published on PGPM in soilless environments,
due to the sterility and lack of necessity for PGPM in hydroponics.
Therefore, there is an immense opportunity to investigate PGPM in
aquaponics. Bartelme et al. (2018) summarized that species such as
Pseudomonas, Bacillus, Enterobacter, Streptomyces, Gliocladium, or
Trichoderma could increase nutrient availability for plants. For
example, the addition of Pseudomonas fluorescens Pf-5 is known to
increase siderophore production in roots found in soil. Side-
rophores are structures which bind to iron and facilitate its trans-
port into plant roots. Therefore, Pf-5 may be a valuable PGPM in
remedying common iron deficiencies in aquaponic systems
(Bartelme et al., 2018; Goddek et al., 2015). It is also possible that
arbuscular mycorrhizae fungi play a key role in phosphorous ab-
sorption in aquaponic systems. Arbuscular mycorrhizae fungi has
been shown to increase phosphorous uptake in low phosphorous
environments, which is significant considering aquaponic systems
can often have low concentrations of phosphorous in the water
(Akiyama et al., 2005; Cerozi and Fitzsimmons, 2017). Schmautz
et al. (2017) sampled different locations of an aquaponic system
and found that although similar microorganisms were present in all
locations, their populations differed. It was found that the biofilter
had high levels of Rhizobiales and Actinobacteria, while roots had
high levels of Burkholderiales, Flavobacteriales, and Pseudomona-
dales. Pseudomonas spp. is a significant microorganism because it is
capable of producing antimicrobial properties as a method of
expansion, which simultaneously protects the surface area they are
growing on from disease, such as root rot caused by Pythium (Avis
et al., 2008; Schmautz et al., 2017). This may be a factor in the ability
of aquaponic plants to mitigate waterborne diseases. It has been
suggested that PGPM of different species can have a synergetic
effect on plant growth when more than one are present at the same
time; however, future studies are needed to clarify these mecha-
nisms (Avis et al., 2008). Speculation of increased plant perfor-
mance from PGPM has led to the development of PGPM culturing.
Cerozi and Fitzsimmons (2016) predicted that plant performance
could increase with increased bacillus strains, as bacillus is known to
make phosphorous more available through mineralization and
solubilisation of precipitates. They found that adding “Sanolife®
PRO-W; 5.0  1010 CFU g1, INVE”, twice a week to their aquaponic
system at 0.02 g of product per liter of water, significantly increased
plant yields and phosphorous content of lettuce, when compared to
lettuce grown in an aquaponic system without added bacillus.
Additionally, it was found that in the system with bacillus
1593
inoculation, ammonia decreased and nitrates were higher, signi-
fying the utilization of nitrogen and possible promotion of nitrify-
ing bacteria (Cerozi and Fitzsimmons, 2016). Similarly, Zou et al.
(2016b) added nitrifying bacteria to improve the nitrogen use ef-
ficiency (NUE) of their aquaponic system. They found that adding
B103 (BIOZYM, USA) (composed of nitrobacteria, denitrifying bac-
teria, bacillus, lactobacillus, and actinomycetes) on a weekly basis
resulted in lettuce yields improving by 15% and NUE increasing by
4.4%. Considering multiple studies on plant improvement through
microflora addition, it is suggested that microflora play a key role in
the success of plants in aquaponic systems. There is however, few
studies which investigate the key mechanisms and species of
microflora, which allow this to happen in aquaponic systems.
Future research on such matters could have significant value in
terms of application for increased crop production with lower re-
quirements of nutrients.
3.1.7. Additional species
Additional aquatic organisms may also be added to different
parts of the system for further benefit. Rakocy et al. (2006) reported
including fingerling tilapia in the clarifier and associated pipes to
remove solid buildups which may lead to clogging. Fang et al.
(2017) attempted to improve NUE by incorporating microalgae
bacteria (consortia) in the bioreactor of an aquaponic system. The
algae aquaponics system had an increase in NUE by 13.8%, an in-
crease in dissolved oxygen in the bioreactor, and lower N2O emis-
sions. Microalgae provides O2 for bacteria to mineralize organic
nutrients, while simultaneously the CO2 produced by bacteria
supports microalgae photosynthesis. Microalgae has also been
shown to reduce ammonia levels in the water compared to bio-
filters containing nitrifying bacteria (Gilles et al., 2014). This may
be a more ideal option for those focussing on the aquaculture
portion of the system for income, as microalgae can be used as a
fish feed or as a biofuel, while simultaneously removing high levels
of nitrogen from the system without taking up a high quantity of
space. Another method of increasing the NUE of aquaponic systems
is adding new species to mitigate dissolved inorganic nitrogen.
Marques et al. (2017) reported using polychaetes (worms) in a sand
filter to decrease organic solids and unavailable nitrogen. They
found that with the addition of Hediste diversicolor (Ragworm)
infused in the sand filter, organic material was decreased by 70%
and dissolved inorganic nitrogen was decreased by 67%.
3.2. Horticulture challenges
Even in well designed and managed aquaponic systems, there
are some fundamental challenges in using the system for plant
production. After the literature review it became evident that there
are four main areas of aquaponics that have been suggested as
limitations to optimizing plant production and resource use effi-
ciency. They are as follows: nitrogen use efficiency (NUE), nutrient
limitations, pH limitations and solid accumulation in the system
water. The specific challenges these categories pose, are described
sequentially, followed by a discussion on their role in future com-
mercial and research based applications in horticulture.
3.2.1. Nitrogen use efficiency
As a result of a highly promoted nitrification process, nitrogen
(NO þ
3 , NH4 ) available for plant uptake is abundant in most aqua-
ponic systems; however, the efficiency at which nitrogen is
assimilated has not been well-recorded in earlier aquaponic pub-
lications. Speculation over the true NUE of aquaponic systems
began to arise after the system became regarded as highly resource
efficient. A number of studies such as Zou et al. (2016a,b), Fang et al.
1594 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
(2017), and Wongkiew et al. (2017a, 2017b), evaluated the NUE of
aquaponic systems, as well as methods that could be used to in-
crease their efficiency. Studies found that on average, aquaponics
has a NUE between 34.4 and 56.6% (Fang et al., 2017; Zou et al.,
2016b). In comparison, 50% of global fertilizer is applied to rice,
wheat and corn, which typically have a NUE below 40% (Canfield
et al., 2010). Other studies have estimated that conventional agri-
culture has, on average, a NUE of 50% (Eickhout et al., 2006). This
would indicate that aquaponics has a similar or possibly lower NUE
than conventional agriculture, despite being renown as a superior
resource efficient system. Fish assimilate 20e30% of nitrogen pro-
vided in fish feed on average, indicating that 70e80% of nitrogen is
released into the water (Hargreaves, 1998; Krom et al., 1995). Of the
70e80% of nitrogen released in the water, only 10e37% is typically
assimilated by plants (Wongkiew et al., 2017b; Zou et al., 2016b).
The remaining 43.4e65.6% is lost through nitrous oxide (N2O)
emissions (1.5e1.9%) (via denitrification, nitrification, and anaer-
obic ammonium oxidation -‘anammox’), ammonia volatilization,
water accumulation, sediment accumulation, solids removal, and
assimilation from other microorganisms (Hu et al., 2015; Zou et al.,
2016b). Although nitrogen deficiency is not a typical problem in
aquaponic systems, increasing the NUE appears to be an area of
interest, based on literature reviewed. NUE can be improved by
increasing the frequency of feeding (increasing feeding frequency
from 8 to 12 times resulted in a 4.9% increase in fish growth and an
11% increase in plant growth) (Liang and Chien, 2013), decreasing
daily feed input (decreasing feed input from 50 g/plant to 35 g/
plant increased NUE by 18.8% in a lettuce system, and by 22.1% in a
pak choi system) (Wongkiew et al., 2017b), using plant species with
higher root biomass (i.e. tomatoes have a NUE 6.9% higher than pak
choi) (Hu et al., 2015), adding nitrifying bacteria (Zou et al., 2016b),
using media beds (Zou et al., 2016b), and using a lower pH (6.0)
(Zou et al., 2016a).
Although current aquaponics do not appear to have a NUE su-
perior to that of other forms of agriculture, the location and form of
unused nitrogen is different from that of conventional agriculture.
For example, nitrogen loss from N2O represents one of the more
detrimental losses of nitrogen in any agriculture system. Although
minimizing N2O has been of interest in aquaponic research, its
production in aquaponic systems is miniscule in comparison to
other contributors. In the US, in 2016, N2O emissions were equiv-
alent to approximately 390 million metric tons of carbon dioxide
equivalent (EPA, 2010). 77% of these emissions originated from
agriculture soil management, where N2O was released through
poor/excessive fertilizer application and burning of agriculture
residues (Eickhout et al., 2006; EPA, 2010). Aquaponics, in com-
parison, does not typically use nitrogen fertilizer, and nitrogen
cannot be lost from weather events. Most of the un-assimilated
nitrogen in aquaponics is retained in the water, sediment or mi-
croorganisms. Furthermore, if the most N2O emitting aquaponic
system published by Zou et al. (2016b) (emits 508.2 ugN/m2/
h ~ 44,520 gN/ha/year) was scaled up across every hectare of arable
land in the United States (152,262,500 ha), the N2O emissions
would be equal to 6.7 million metric tons N/year, significantly lower
than the current 300 million metric tons produced by current
agriculture (EPA, 2010). In appears that the need to improve NUE in
aquaponic systems is based on the system not having a superior
NUE to other forms of agriculture, despite being regarded as a
highly efficient system. However, the release of nitrogen com-
pounds into the environment is still minimal in comparison to
conventional agriculture. In summary, aquaponics NUE can be
improved; however, NUE does not appear to be a limiting challenge
for the expansion of commercial aquaponics. A more crucial
limiting challenge in aquaponics is the ratio of nutrients available
for plants to uptake.
3.2.2. Nutrient limitations
In aquaponic systems the four most common limiting essential
nutrients for plants in the solution are Ca, K, Mg and Fe (Rakocy,
2003; Villarroel et al., 2011). Since fish have minimal re-
quirements of many metal ions (Fe, Mn, Mg, Cu), and lower re-
quirements for K (only 1% of composition) (Seawright et al., 1998),
these nutrients are accordingly low in fish feed, and therefore low
in aquaculture effluent (IAFFD, 2018; Rakocy, 2003). The major
ingredient in most fish feed is fish meal (Cerozi and Fitzsimmons,
2017a,b). Fish meal is full of amino acids (organic forms of nitro-
gen) and phosphorous, but lacks K and several micronutrients (Fe,
Mn, Cu) required by plants (IAFFD, 2018; Savidov et al., 2007). These
nutrients are made further unavailable for plant uptake, through
chemical antagonisms in the system and non-optimal system water
pH. To prevent deficiencies in these nutrients, some aquaponic
systems supplement synthetic salts (i.e. potassium hydroxide) into
the system water (Rakocy, 2003), or apply a foliar spray (Roosta,
2014). Although aquaponic systems aim to rely as little as
possible on synthetic fertilizer for plant growth, it is possible to
make up nutrient deficiencies and increase yield significantly with
minimal synthetic fertilizer application.
Of the limiting nutrients in aquaponic systems, K has been re-
ported to be one of the more significant. Graber and Junge (2009)
found that aquaponic water had on average 45-fold less K than
hydroponic solutions. Considering that K is the fifth most up taken
nutrient, represents as high as 10% of plant tissue (Seawright et al.,
1998), and plays an essential role in nutrient transport (specifically
Fe and NHþ 4 transport), enzyme activation (phosphoenolpyruvate
carboxylase (PEP-case) glutamine synthetase (GS)), and moder-
ating osmotic potential, potassium deficiency can be detrimental to
plant growth and yield (Gajdanowicz et al., 2011; Gierth and Ma €ser,
2007). Two methods of overcoming K deficiencies are incorpo-
rating K into the system water as a salt, or applying to plants as a
foliar spray. Roosta (2014) found that a K foliar spray on parsley
increased yields by up to 60.7% as compared to parsley without a
foliar spray. Gullian Klanian et al. (2018) found that K added to the
solution improved tomato fruit yield, while K in the foliar fertil-
ization improved plant growth. Alternatively, UVI systems increase
K in the water by adding potassium hydroxide (KOH) (Rakocy et al.,
2004b; 2006). KOH has the secondary purpose of increasing or
maintaining a neutral pH in acidic aquaponic systems. K also affects
the uptake of other nutrients, specifically Fe. Fe is a nutrient already
typically deficient in aquaponic systems; therefore, its supple-
mentation is crucial if K is also low. Hydroponic crops typically
receive Fe in an available form such as soluble Fe-EDTA or Fe-
EDDHA at a concentration between 2 and 5 mg/L (Goddek et al.,
2015; Radzki et al., 2013). In aquaponics Fe can be found in the
water at concentrations of 0.2e2.5 mg/L (Bartelme et al., 2018;
Goddek et al., 2015). In addition to the minimal input of Fe into
aquaponic systems, Fe can be made further unavailable through the
speciation of ferrous iron (Fe2þ) (highly soluble across rhizoplanes
of roots) to ferric iron (Fe3þ) (less soluble across rhizoplane of
roots), via ionic reactions and hydroxyl radicals in the system water
(Bartelme et al., 2018; Rose and Waite, 2002). Roosta and
Mohsenian (2012) investigated the impact of varying Fe sources
as a foliar spray for peppers in an aquaponic system. They found
that a foliar spray containing FeSO4 led to higher vegetative and
reproductive growth in peppers, compared to foliar spays con-
taining Fe-EDDHA, and Fe-EDTA. Alternatively, the UVI systems add
chelated Fe2þ into their system water at a rate of 2 mg/L, every three
weeks for their 214 m2 growing area (Rakocy et al., 2010). Rakocy
(2003) suggests adding iron as Fe-DTPA as it remains stable at a
pH of 7.0. Additionally, the fish species present in the system will
dictate whether Fe addition is suitable. For example,
O. mossambicus fingerlings have a LC50 of 8.00e9.38 mg/L of Fe,
 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
whereas C. carpio has a LC50 of 1.22e2.25 mg/L of Fe for 24e96 h
(Mashifane and Moyo, 2014). Similar to Fe, Mn, which may also be
deficient in aquaponic systems, can cause chlorosis when deficient
(Buhmann et al., 2015). Buhmann et al. (2015) found that Mn
addition only increased plant growth when it was included with
Fe-EDHHA in a saltwater aquaponic system. Another nutrient
commonly supplemented in aquaponics is Mg. Mg has been re-
ported to be concentrated around 4 mg/L in aquaponics (Villarroel
et al., 2011), which is significantly lower than 24e50 mg/L found in
lettuce hydroponics (Sonneveld and Voogt, 2009; Resh, 2012). Mg
can be supplemented as dolomite (CaMg(CO3)2) which also doubles
as a base to raise the pH in acidic systems (Rakocy, 2003). There are
limited studies on the severity of Ca, Mg or Mn deficiencies on
aquaponic plants. Future studies should investigate if these nutri-
ents are causing growth limitations, and if so, the effects of addi-
tional Ca, Mg or Mn in the form of a foliar spray or system addition
should also be studied.
Another nutrient which is sometimes un-proportional in
aquaculture effluent is phosphorous (P). A number of studies, such
as Diem et al. (2017) or Monsees et al. (2017a), found that total P
accumulated over time in aquaponic systems growing lettuce.
Excess P can create antagonisms with micronutrients, such as Zn
(Cerozi and Fitzsimmons, 2017a,b). Alternatively, several other
studies have found a lack of total P in their systems, well below
17 mg/L in some cases (Endut et al., 2010; Goddek et al., 2015). This
may be the result of P precipitating as solid particles, and then
becoming unavailable through the separation of solid particles in
filtration tanks. If there is a high level of Ca in the system water
(common in areas using water from basic limestone aquifers), P,
specifically orthophosphate, will precipitate to form calcium
phosphate (Ca3(PO4)2) or dicalcium phosphate (CaHPO4) at a
neutral pH (Rakocy et al., 2006; Seawright et al., 1998). Ca3(PO4)2 is
a solid which can be filtered out from the system and is also not
available for plant uptake (Rakocy, 2003). P deficiencies can lead to
stunted growth, specifically in heavier feeding crops such as fruits
or vegetables (Cerozi and Fitzsimmons, 2017a,b). Despite signifi-
cantly lower P concentrations, Blidariu et al. (2013) found that
lettuce grown in aquaponic water containing P concentrations of
3.2e3.6 mg/L had higher P tissue content than lettuce grow in field
studies. This may be a result of increased P availability in low P
environments by PGPMs, such as arbuscular mycorrhizae fungi as
mentioned in section 3.1.6 (Akiyama et al., 2005; Bartelme et al.,
2018). Cerozi and Fitzsimmons (2017a,b) found that P use effi-
ciency was relatively high (71.7% total, 42.3% in fish and 29.4%
plants), in comparison to NUE.
Despite aquaponic water samples being identified as having less
nutrients in comparison to standard hydroponic water (Bitts anszky
et al., 2016), vegetative plants in aquaponics systems have been
reported to have similar or equal yields to those plants grown hy-
droponically. One possible explanation for such a phenomenon, is
that the nutrients in aquaponic water are in an organic state, as
opposed to a sterile ionic state found in most of the hydroponic
water. This organic source of nutrients may, A) reduce the mea-
surement of nutrients actually in the water (Rakocy, 2003), and B)
promote growth by stimulating natural growing conditions as
opposed to sterile hydroponic conditions (Bӧhme, 1999; Goddek
et al., 2015). These organic factors include humic acids (fulvic
acid) (Canellas et al., 2009; Haghighi et al., 2012), indole-3-acetic
acid (IAA) (Mangmang et al., 2015), rhizobacteria and arbuscular
fungi (Bartelme et al., 2018). For example Pantanella et al. (2012)
and Delaide et al. (2016) found no difference in yields of lettuce
compared to lettuce grown in hydroponic systems, despite the
aquaponic water of Delaide et al. (2016) having 23% NO 2
3 , 15% PO4 ,
27% Kþ and 8% Ca2þ, of what was present in the hydroponic water
used in their study.
1595
It is possible to manipulate the nutrient profile in the aquacul-
ture effluent by changing the diet fed. Seawright et al. (1998) were
the first to investigate the nutrient profile created by conventional
fish feed, and the first to propose recommendations for feed ma-
nipulations to provide better nutrients for plant production. They
found that K, Mg, Mn, P, Na, and Zn were nutrients which could be
manipulated in the feed to increase plant productivity, while Fe and
Cu would not be able to be manipulated. A more recent study by
Cerozi and Fitzsimmons (2017a) investigated the use of a plant
based feed with phytase. Plant proteins typically have P stored in
the form of phytate, which is unavailable for fish to assimilate. The
addition of phytase to the diet allows phytate to be broken down
and assimilated in the fish. The study found that adding phytase in
fish food increased growth in fish but lowered overall dissolved
phosphorus in the water. This, however, did not affect plant growth,
indicating that a feed adaptation such as phytase addition can in-
crease P use efficiency (Cerozi and Fitzsimmons, 2017a,b). Plant
based fish feeds are a more sustainable form of feed and will most
likely increase in the aquaculture industry, considering that con-
ventional fish feeds are primarily fish meal, which is expensive,
in shortage and an environmentally degrading feed component
(Cerozi and Fitzsimmons, 2017a,b; Goddek et al., 2015). To the au-
thor's knowledge, there is no other comprehensive studies which
investigate the effects of a custom fish feed in comparison to a
conventional fish feed in an aquaponic system. Future studies
should investigate alternative fish feeds, which produce effluent
that is higher in K and Mg. In summary, suboptimal nutrient con-
centrations compared to standard hydroponic solutions, appears to
be a major limitation for growing crops with higher nutrient re-
quirements. Although there are several studies identifying methods
to improve crop yields through foliar sprays or adding fertilizer to
the water, there is yet to be research which investigates alternative
methods of increasing nutrient concentrations in aquaponic solu-
tion without using synthetic material, a fundamental pillar of sus-
tainability in aquaponics.
3.2.3. pH
The three main organisms in aquaponic systems: fish, nitrifying
bacteria, and plants, have different optimal pH ranges. Nile tilapia
have an optimal pH between 7.0 and 9.0; the three major nitrifying
bacteria genera Nitrobacter, Nitrosomonas and Nitrospira have
optimal pH ranges of 7.5, 7.0e7.5 and 8.3, respectively (Antoniou
et al., 1990; Goddek et al., 2015; Rakocy, 2003); and hydroponic
plants perform optimally in a pH range of 5.8e6.2 (Cooper, 1979;
Sonneveld and Voogt, 2009). Given these obvious differences in
optimal pHs, no one organism's growth can be optimized without
another's being compromised, illustrating one of the major chal-
lenges in any aquaponic system. Many aquaponic review articles
have recommended an optimal pH level, based on a compromise
between optimal fish, bacteria and plant performance. These
optimal ranges vary depending on what aspect of aquaponics the
author found to be more valuable. For example, Rakocy (2003),
Tyson et al. (2008) and Goddek et al. (2015) suggested optimal
pH ranges for aquaponics of 7.0, 6.8e7.0, and 7.5e8.0, respectively.
Most authors recommend a pH range that is more neutral, opti-
mizing the nitrification process (pH < 7.0) over nutrient availability
for plants. Alternatively, Tyson et al. (2008) used a lower pH of 6.0
to enhance nutrient uptake by plants; however, this resulted in
increased fish mortality and a significant decrease in nitrification.
In mature aquaponic systems, water pH typically becomes acidic
over time. This is the result of acid (Hþ) production from the
nitrification of ammonia, which is continuously excreted from the
gills of fish (Rakocy et al., 2004). Although most plants in aquaponic
systems release hydroxide eOH or bicarbonate HCO 3 when
assimilating nitrate, the basic ions do not sufficiently counter the
1596 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
hydrogen released from nitrification (Goddek et al., 2015). This
acidic pH can be countered with the addition of KOH or Ca(OH) to
the system water, as commonly conducted in UVI systems (Rakocy,
2003). Although acidic pH levels may be considered a challenge,
Rakocy (2003) outlined that if pH is remaining constant in a mature
system, it may be a result of excessive denitrification. If excess
denitrification is occurring, NUE will decrease along with available
nitrogen for plant uptake. This also prevents the addition of
Ca(OH)2 or KOH to be added to the system, which may lead to
deficiencies in Ca or K. Alternatively, others have proposed the use
of technology, such as a fluidized lime bed reactor, to counter an
acidic pH range (Goddek et al., 2015). A fluidized lime bed reactor
would supply a set quantity of dissolved limestone (CaCO3) directly
into the system water which would produce hydroxide anions to
increase pH. Although there are numerous publications on the
impact of pH in aquaponics, it appears as though it is not a major
limiting factor if a compensated range (6.7e7) is used to satisfy
both plants and fish to some degree. Alternatively, the use of DAS,
as described in Section 2, is one solution to having varying optimal
pH ranges. Apart from nutritional related limitations, aquaponics is
also burdened with the challenge of handling solid accumulation in
the system.
3.2.4. Solids
Build ups of organic material (un-eaten feed, algae, fungi, fish
sludge) can be detrimental to aquaponic systems. Although a small
build-up of solid materials is necessary for providing a constant
concentration of nutrients through mineralization (via minerali-
zation tanks or filtration tanks), excessive solid build up can be
harmful. Organic build ups or formation of sludge creates anaerobic
environments which can cause anaerobic bacteria to release carbon
dioxide, ammonia, hydrogen sulfide and methane, which are toxic
to fish (Rakocy et al., 2006). Furthermore, if solids build up around
the roots of plants they can create an anaerobic environment and
inhibit oxygen to plant roots, which they require for nutrient up-
take mechanisms (Rakocy et al., 2006). Lowered dissolved oxygen
(<7 mg/L) around the root zone also increases susceptibility to root
rot, caused by Pythium (Cherif et al., 1997). Anaerobic solid build
ups also have the possibility to create “off-flavours”. Off flavours are
typically secondary metabolites, such as geosmin or 2-
methylisoborneol produced by Streptomyces, which can grow
when there is an accumulation of organic material containing
phosphorous (Rurangwa and Verdegem, 2015). Although this is a
concern for some producers and consumers, a study investigating
microbial communities in the Wa €denswil aquaponic facility found
no Streptomyces present, nor was it reported in any of the articles
reviewed, indicating that this may not be a prevalent problem
(Schmautz et al., 2017).
Since aquaponic systems contain a high level of living micro-
organisms, it is possible that pathogenic microbes or aquatic pests
could develop, particularly if solids accumulate. One example is the
zooplankton pest. Zooplankton, specifically ostracods, pose a threat
to aquaponic systems by consuming root hairs, preventing nutrient
uptake and inhibiting growth (Rakocy et al., 2006). Andriani et al.
(2018) found that the most common zooplankton in their aqua-
ponic systems were Brachionus sp. and Epistylis sp, the latter being a
microorganism that causes disease in fish. Another pest related
organism that can develop from solid accumulation is A.ocellatum;
an “obligate ecto-parasitic, dinflagellate” which targets marine fish
(Nozzi et al., 2016). Fortunatley, solid acumulation can be mitigated
in most systems through sludge removing clarifiers or filtration
tanks which can be cleaned (Goddek et al., 2016; Rakocy et al.,
2006). If a disease or pest were to outbreak in an aquaponic sys-
tem, there would be limited options to remediate the situation,
since pesticides and antibiotics cannot be used on plants/fish as
their effects are either unknown or harmful (Goddek et al., 2015).
However, based on the literature review conducted here, most
studies investigating aquaponics have not reported any detrimental
disease out breaking in their system. It is possible that this is a
result of beneficial microbial communities living in the rhizosphere
of plant roots which have antimicrobial properties, allowing them
to prevent disease (Gravel et al., 2015; Schmautz et al., 2017).
Another concern is the physical presence of microorganisms on
marketable aquaponic produce, as their presence may be high in
the water. There is a number of restrictions on how many coliforms
are allowed in water, based on different global locations as
described in Pantanella et al. (2015). A possible method of
decreasing these microbes is the use of UV light. Pantanella et al.
(2015) found that ultraviolet light decreased bacteria by a
1000 CFU/ml in the fish tanks, lowering the coliform count below
what was previously above the World Health Organization stan-
dard (1989). Few other studies have reported on the presence of
microbes on marketable produce, and therefore future research
should be conducted on such matters. Since aquaponics produces
food in close proximity to fish waste, the safety and sterility of
aquaponics produce is a concern. Aquaponics lacks a regulating
body to certify aquaponic products are truly aquaponically grown. A
certification system for aquaponic produce would greatly benefit
the commercial industry as it would ensure products are free of
pathogens and safe for consumption, allow products to be mar-
keted at a higher price based on certification, and deter pseud-
aquaponic cultivation (those that use >50% synthetic fertilizer).
This would further legitimize aquaponic produce for the consumer,
providing a guarantee that the product has been sustainably pro-
duced. Such factors may increase the feasibility of aquaponic pro-
duce in the commercial market place and encourage sustainable
consumption.
4. Conclusion
Aquaponic systems carry great potential to overcome several
sustainability challenges in the agriculture sector; primarily the
ability to produce high yields with minimal added nutrients, while
also greatly reducing nutrient discharge and water loss from
aquaculture. The growing interest in sustainable agriculture sys-
tems such as aquaponics, is illustrated in this review by the expo-
nential release of aquaponic publications in the last 3 years. From
these recent developments, clear trends, implications, and needs
for future research on system design, hydroponic components,
optimal fish, plant and microorganism species have emerged, and
are as follows:
 It appears that a movement from CAS to DAS is primarily based
on optimizing the horticulture portion of aquaponics but lacks
evidence that the change in systems will be as economical and
sustainably compromising, on account of increased required
space and fertilizer for DAS. Given that commercial aquaponics
is expanding rapidly, it is possible that systems designs are
rapidly adapted based on unproven premises, which may
endanger the sustainable effectiveness of these systems in the
sector. This potential issue can be clarified by well-designed
experiments investigating the economics and sustainability
between CAS and DAS in a commercial context.
 Natural variations, management techniques, and application of
hydroponic components in aquaponic systems make it difficult
to derive conclusions on which component is optimal. For small
scale and research aquaponic systems, a media bed hydroponic
component appears to be the most successful based on its ability
 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
to grow a variety of plants and mitigate the use of a biofilter. For
commercial aquaponic systems, a DWC component appears to
be optimal based on its low environmental impact, higher water
use efficiency, maximized root to water contact and consistent
high plant yields.
 Tilapia, followed by Carp and African Catfish appear to be the
most successful fish species used in aquaponic systems. These
fish are successful as a result of their ability to handle high levels
of nitrate and low oxygen. There has yet to be a study which
investigates the benefits of polyculture in aquaponic systems.
Considering polyculture may create a more optimally nutrient
balanced solution for plant growth, future research on this topic
could have substantial value.
 Leafy greens such as varieties of lettuce, mint, and basil appear
to be the most successful plant species in aquaponics, as a result
of their low nutrient requirements, universal demand, and
economical value in aquaponic systems. There are few studies
referencing the use of aquaponics for flowering crop production.
Evaluating the use of aquaponics for a variety of flowering
species, may allow the expansion of aquaponics into the flori-
culture industry.
 It is possible Nitrospira has a major role in the nitrification
process in aquaponics, over past thought of nitrifiers such as
Nitrobacter and Nitrosomonas. Future studies should investigate
the role of nitrifying bacteria in aquaponics through their NUE
and interactions with plant roots and surrounding microor-
ganisms. Such studies may provide information relating to im-
provements in nutrient extraction from aquaculture waste.
 PGPM in aquaponics are often suggested to be the reason plants
can mitigate disease and have equal yields to hydroponics,
despite lower nutrient levels. There are few studies on PGPM in
aquaponic studies. Future PGPM studies on aquaponics will be
imperative to understanding the underlying mechanisms of
nutrient dynamics in aquaponics systems, which could be
valuable for further improvement in all forms of agriculture.
Given the energy intensive requirements of fertilizer, the impact
of growing plants with minimal fertilizer can greatly reduce the
carbon footprint of crops grown. This review suggests that
aquaponics is an ideal system to observe and understand the
nature of PGPM, which may allow for their application in other
growing methods.
These trends and research suggestions can help both industry
and academia establish what is already successful in aquaponics
and what research will be most influential. From a horticulture
perspective, the two following points appear to be the most
limiting for the industry and require future research:
 Aquaponics largest horticulture challenge is providing balanced
nutrients for heavy feeding plants. Specifically, aquaponic so-
lution has been found to have insufficient K, Mg, Ca and Fe for
some plants. Several articles have found that these nutrient
limitations can be overcome with nutrient additions to the
system, or foliar sprays, however future studies should investi-
gate if nutrient levels in aquaponic water can be optimized
through custom fish feed or the use of polyculture, as such a
solution would minimize the use of synthetic fertilizers. Future
studies are also needed to determine optimal Ca, Mg and Mn
additions for plants in aquaponic systems.
 There is a lack of standards to which aquaponic goods can be
sold with ensured quality, safety, and verification of true aqua-
ponic cultivation. A clear set of aquaponic standards should be
developed to help create a more established market for aqua-
ponic products..
1597
Acknowledgement
The authors would like to acknowledge Natural Sciences and
Engineering Research Council of Canada.
References
Adler, P.R., Harper, J.K., Wade, E.M., Takeda, F., Summerfelt, S.T., 2000. Economic
analysis of an aquaponic system for the integrated production of rainbow trout
and plants. Int. J. Recirc. Aquac. 1, 15e34. https://doi.org/10.21061/ijra.v1i1.1359.
Akiyama, K., Matsuzaki, K.I., Hayashi, H., 2005. Plant sesquiterpenes induce hyphal
branching in arbuscular mycorrhizal fungi. Nature 435, 824e827. https://doi.
org/10.1038/nature03608.
Andriani, Y., Dhahiyat, Y., Zahidah, Subhan, U., Iskandar, Zidni, I., Mawardiani, T.,
2018. Effect of water irrigation volume on Capsicum frutescens growth and
plankton abundance in aquaponics system. In: IOP Conf. Series: Earth and
Environmental Science, pp. 1e10. https://doi.org/10.1088/1755-1315/139/1/
012001.
Antoniou, P., Hamilton, J., Koopman, B., Jain, R., Holloway, B., Lyberatos, G.,
Svoronos, S.A., 1990. Effect of temperature and ph on the effective maximum
specific growth rate of nitrifying bacteria. Water Res. 24, 97e101. https://doi.
org/10.1016/0043-1354(90)90070-M.
Avis, T.J., Gravel, V., Antoun, H., Tweddell, R.J., 2008. Multifaceted beneficial effects
of rhizosphere microorganisms on plant health and productivity. Soil Biol.
Biochem. 40, 1733e1740. https://doi.org/10.1016/j.soilbio.2008.02.013.
Bailey, D.S., Ferrarezi, R.S., 2017. Valuation of vegetable crops produced in the UVI
commercial aquaponic system. Aquac. Reports 7, 77e82. https://doi.org/10.
1016/j.aqrep.2017.06.002.
Bartelme, R.P., McLellan, S.L., Newton, R.J., 2017. Freshwater recirculating aquacul-
ture system operations drive biofilter bacterial community shifts around a
stable nitrifying consortium of ammonia-oxidizing archaea and comammox
Nitrospira. Front. Microbiol. 8, 1e18. https://doi.org/10.3389/fmicb.2017.00101.
Bartelme, R.P., Oyserman, B.O., Blom, J.E., Sepulveda-Villet, O.J., Newton, R.J., 2018.
Stripping away the soil: plant growth promoting microbiology opportunities in
aquaponics. Front. Microbiol. 9, 1e7. https://doi.org/10.3389/fmicb.2018.00008.
Bitts
anszky, A., Uzinger, N., Gyulai, G., Mathis, A., Junge, R., Villarroel, M., Kotzen, B.,
Ko}míves, T., 2016. Nutrient supply of plants in aquaponic systems. Ecocycles 2,
17e20. https://doi.org/10.19040/ecocycles.v2i2.57.
Blackburne, R., Vadivelu, V.M., Yuan, Z., Keller, J., 2007. Kinetic characterisation of an
enriched Nitrospira culture with comparison to Nitrobacter. Water Res. 41,
3033e3042. https://doi.org/10.1016/j.watres.2007.01.043.
Blidariu, F.C., Drasovean, A., Grozea, A., 2013. Evaluation of phosphorus level in
green lettuce conventional grown under natural conditions and aquaponic
system. Bull. UASVM Anim. Sci. Biotechnol. 70, 128e135.
Bosma, R.H., Lacambra, L., Landstra, Y., Perini, C., Poulie, J., Schwaner, M.J., Yin, Y.,
2017. The financial feasibility of producing fish and vegetables through aqua-
ponics. Aquacult. Eng. 78, 146e154. https://doi.org/10.1016/j.aquaeng.2017.07.
002.
Buhmann, A.K., Waller, U., Wecker, B., Papenbrock, J., 2015. Optimization of
culturing conditions and selection of species for the use of halophytes as bio-
filter for nutrient-rich saline water. Agric. Water Manag. 149, 102e114. https://
doi.org/10.1016/j.agwat.2014.11.001.
Bӧhme, M., 1999. Effects of lactate, humate and Bacillus subtilis on the growth of
tomato PLants in hydroponic systems. Proc. Int. Sym. Grow. Media Hydroponics
481, 231e239.
Canellas, L.P., Spaccini, R., Piccolo, A., Dobbss, L.B., Okorokova-Façanha, A.L.,
Santos, G.D.A., Olivares, F.L., Façanha, A.R., 2009. Relationships between
chemical characteristics and root growth promotion of humic acids isolated
from Brazilian oxisols. Soil Sci. 174, 611e620. https://doi.org/10.1097/SS.
0b013e3181bf1e03.
Canfield, D.E., Glazer, A.N., Falkowski, P.G., 2010. The evolution and future of earth's
nitrogen cycle. Science 84 330, 192e196. https://doi.org/10.1126/science.
1186120.
Cerozi, B. da S., Fitzsimmons, K., 2017a. Phosphorus dynamics modeling and mass
balance in an aquaponics system. Agric. Syst. 153, 94e100. https://doi.org/10.
1016/j.agsy.2017.01.020.
Cerozi, B. da S., Fitzsimmons, K., 2017b. Effect of dietary phytase on phosphorus use
efficiency and dynamics in aquaponics. Aquacult. Int. 25, 1227e1238. https://
doi.org/10.1007/s10499-016-0109-7.
Cerozi, B. da S., Fitzsimmons, K., 2016. Use of Bacillus spp. to enhance phosphorus
availability and serve as a plant growth promoter in aquaponics systems. Sci.
Hortic. 211, 277e282. https://doi.org/10.1016/j.scienta.2016.09.005.
Cherif, M., Tirilly, Y., Belanger, R.R., 1997. Effect of oxygen concentration on plant
growth, lipid peroxidation, and receptivity of tomato roots to Pythium under
hydroponic conditions. Eur. J. Plant Pathol. 103, 255e264. https://doi.org/10.
1023/A:1008691226213.
Cooper, A., 1979. The ABC of NFT, first ed. Grower Books, London.
Daims, H., Lebedeva, E.V., Pjevac, P., Han, P., Herbold, C., Albertsen, M., Jehmlich, N.,
Palatinszky, M., Vierheilig, J., Bulaev, A., Kirkegaard, R.H., Von Bergen, M.,
Rattei, T., Bendinger, B., Nielsen, P.H., Wagner, M., 2015. Complete nitrification
by Nitrospira bacteria. Nature 528, 504e509. https://doi.org/10.1038/
nature16461.
Danaher, J.J., Shultz, R.C., Rakocy, J.E., Bailey, D.S., 2013. Alternative solids removal
1598 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
for warm water recirculating raft aquaponic systems. J. World Aquacult. Soc. 44,
374e383. https://doi.org/10.1111/jwas.12040.
Delaide, B., Goddek, S., Gott, J., Soyeurt, H., Jijakli, M.H., 2016. Lettuce (Lactuca sativa
L. var. Sucrine) growth performance in complemented aquaponic solution
outperforms hydroponics. Water 8, 1e11. https://doi.org/10.3390/w8100467.
Diem, T.N.T., Konnerup, D., Brix, H., 2017. Effects of recirculation rates on water
quality and Oreochromis niloticus growth in aquaponic systems. Aquacult. Eng.
78, 95e104. https://doi.org/10.1016/j.aquaeng.2017.05.002.
Diver, S., 2006. Aquaponics d integration of hydroponics with aquaculture. ATTRA
Natl. Sustain. Agric. Infromation Serv 56, 1e28.
Eickhout, B., Bouwman, A.F., van Zeijts, H., 2006. The role of nitrogen in world food
production and environmental sustainability. Agric. Ecosyst. Environ. 116, 4e14.
https://doi.org/10.1016/j.agee.2006.03.009.
El-Sayed, A.F.M., 2006. Tilapia Culture. CAB eBooks, Oceanography Department,
Faculty of Science, Alexandria University, Alexandria, Egypt. https://doi.org/10.
1079/9780851990149.0000.
Endut, A., Jusoh, A., Ali, N., Wan Nik, W.B., Hassan, A., 2010. A study on the optimal
hydraulic loading rate and plant ratios in recirculation aquaponic system. Bio-
resour. Technol. 101, 1511e1517. https://doi.org/10.1016/j.biortech.2009.09.040.
Engle, C.R., 2015. Economics of aquaponics. SRAC Publ. - South. Reg. Aquac. Cent. No.
5006, 1e4.
EPA, 2010. Methane and Nitrous Oxide Emissions from Natural Sources. U.S. Envi-
ronmental Protection Agency, Washington, DC, USA.
Fang, Y., Hu, Z., Zou, Y., Zhang, J., Zhu, Z., Zhang, J., Nie, L., 2017. Improving nitrogen
utilization efficiency of aquaponics by introducing algal-bacterial consortia.
Bioresour. Technol. 245, 358e364. https://doi.org/10.1016/j.biortech.2017.08.
116.
FAO, 2005. AQUASTAT Survey, Irrigation in Africa in Figures. FAO, Rome, Italy.
Food and Agriculture Organization of the United Nations, 2018. The State of World
Fisheries and Aquaculture. Rome.
Food and Agriculture Organization of the United Nations, 1988. Definition of
aquaculture. In: Seventh Session of the IPFC Working Party of Expects on
Aquaculture, pp. 1e3.
Forchino, A.A., Lourguioui, H., Brigolin, D., Pastres, R., 2017. Aquaponics and sus-
tainability: the comparison of two different aquaponic techniques using the Life
Cycle Assessment (LCA). Aquacult. Eng. 77, 80e88. https://doi.org/10.1016/j.
aquaeng.2017.03.002.
Gajdanowicz, P., Michard, E., Sandmann, M., Rocha, M., Correa, L.G.G., Ramirez-
Aguilar, S.J., Gomez-Porras, J.L., Gonzalez, W., Thibaud, J.-B., van Dongen, J.T.,
Dreyer, I., 2011. Potassium (Kþ) gradients serve as a mobile energy source in
plant vascular tissues. Proc. Natl. Acad. Sci. Unit. States Am. 108, 864e869.
https://doi.org/10.1073/pnas.1009777108.
Gierth, M., M€ aser, P., 2007. Potassium transporters in plants - involvement in
Kþacquisition, redistribution and homeostasis. FEBS Lett. 581, 2348e2356.
https://doi.org/10.1016/j.febslet.2007.03.035.
Gilles, S., Ismin ~ o, R., Sa
nchez, H., David, F., Nún ~ ez, J., Dugue , R., Darias, M.J.,
Ro€ mer, U., 2014. An integrated closed system for fish-plankton aquaculture in
Amazonian fresh water. Animal 8, 1319e1328. https://doi.org/10.1017/
S1751731114001165.
Goda, A.M.A.-S., Essa, M.A., Hassaan, M.S., Sharawy, Z., 2015. Bio economic features
for aquaponic systems in Egypt. Turk. J. Fish. Aquat. Sci. 15, 525e532. https://
doi.org/10.4194/1303-2712-v15.
Goddek, S., Delaide, B., Mankasingh, U., Ragnarsdottir, K.V., Jijakli, H.,
Thorarinsdottir, R., 2015. Challenges of sustainable and commercial aquaponics.
Sustain. Times 7, 4199e4224. https://doi.org/10.3390/su7044199.
Goddek, S., Keesman, K.J., 2018. The necessity of desalination technology for
designing and sizing multi-loop aquaponics systems. Desalination 428, 76e85.
https://doi.org/10.1016/j.desal.2017.11.024.
Goddek, S., Schmautz, Z., Scott, B., Delaide, B., Keesman, K., Wuertz, S., Junge, R.,
2016. The effect of anaerobic and aerobic fish sludge supernatant on hydroponic
lettuce. Agronomy 6, 1e12. https://doi.org/10.3390/agronomy6020037.
Graber, A., Junge, R., 2009. Aquaponic Systems: nutrient recycling from fish
wastewater by vegetable production. Desalination 246, 147e156. https://doi.
org/10.1016/j.desal.2008.03.048.
Gravel, V., Dorais, M., Dey, D., Vandenberg, G., 2015. Fish effluents promote root
growth and suppress fungal diseases in tomato transplants. Can. J. Plant Sci. 95,
427e436. https://doi.org/10.4141/cjps-2014-315.
Gullian Klanian, M., Delgadillo Diaz, M., Aranda, J., Rosales Jua rez, C., 2018. Inte-
grated effect of nutrients from a recirculation aquaponic system and foliar
nutrition on the yield of tomatoes Solanum lycopersicum L. and Solanum
pimpinellifolium. Environ. Sci. Pollut. Res. 25, 17807e17819. https://doi.org/10.
1007/s11356-018-1817-5.
Haghighi, M., Kafi, M., Fang, P., 2012. Photosynthetic activity and N metabolism of
lettuce as affected by humic acid. Int. J. Veg. Sci. 18, 182e189. https://doi.org/10.
1080/19315260.2011.605826.
Hargreaves, J.A., 1998. Nitrogen biogeochemistry of aquaculture ponds. Aquaculture
166, 181e212. https://doi.org/10.1016/S0044-8486(98)00298-1.
Hu, Z., Lee, J.W., Chandran, K., Kim, S., Brotto, A.C., Khanal, S.K., 2015. Effect of plant
species on nitrogen recovery in aquaponics. Bioresour. Technol. 188, 92e98.
https://doi.org/10.1016/j.biortech.2015.01.013.
IAFFD, 2018. Feed Ingredient Composition Database [WWW Document]. http://
www.iaffd.com/home.html?v¼4.01.
Jiang, Q., Dilixiati, A., Zhang, W., Li, W., Wang, Q., Zhao, Y., Yang, J., Li, Z., 2014. Effect
of nitrite exposure on metabolic response in the freshwater prawn Macro-
brachium nipponense. Cent. Eur. J. Biol. 9, 86e91. https://doi.org/10.2478/
s11535-013-0167-4.
Junge, R., Ko €nig, B., Villarroel, M., Komives, T., Jijakli, M.H., 2017. Strategic points in
aquaponics. Water 9, 1e9. https://doi.org/10.3390/w9030182.
Khandaker, M., Kotzen, B., 2018. The potential for combining living wall and vertical
farming systems with aquaponics with special emphasis on substrates. Aqua-
cult. Res. 49, 1454e1468. https://doi.org/10.1111/are.13601.
Kloas, W., Groß, R., Baganz, D., Graupner, J., Monsees, H., Schmidt, U., Staaks, G.,
Suhl, J., Tschirner, M., Wittstock, B., Wuertz, S., Zikova, A., Rennert, B., 2015.
A new concept for aquaponic systems to improve sustainability, increase pro-
ductivity, and reduce environmental impacts. Aquac. Environ. Interact. 7,
179e192. https://doi.org/10.3354/aei00146.
Knaus, U., Palm, H.W., 2017. Effects of the fish species choice on vegetables in
aquaponics under spring-summer conditions in northern Germany (Mecklen-
burg Western Pomerania). Aquaculture 473, 62e73. https://doi.org/10.1016/j.
aquaculture.2017.01.020.
Kong, Y., Zheng, Y., 2014. Potential of producing Salicornia bigelovii hydroponically
as a vegetable at moderate NaCl salinity. Hortscience 49, 1154e1157. https://doi.
org/10.1139/b03-086.
Ko€nig, B., Janker, J., Reinhardt, T., Villarroel, M., Junge, R., 2018. Analysis of aqua-
ponics as an emerging technological innovation system. J. Clean. Prod. 180,
232e243. https://doi.org/10.1016/j.jclepro.2018.01.037.
Krom, M.D., Ellner, S., van Rijn, J., Neori, A., 1995. Nitrogen and phosphorus cycling
and transformations in a prototype “non-polluting” integrated mariculture
system, Eilat, Israel. Mar. Ecol. Prog. Ser. 118, 25e36. https://doi.org/10.3354/
meps118025.
Lennard, W.A., 2015. AQUAPONICS: a nutrient dynamic process and the relationship
to fish feeds. J. World Aquac. Soc. September 20e23.
Lennard, W.A., Leonard, B.V., 2006. A comparison of three different hydroponic sub-
systems (gravel bed, floating and nutrient film technique) in an Aquaponic test
system. Aquacult. Int. 14, 539e550. https://doi.org/10.1007/s10499-006-9053-
2.
Liang, J.Y., Chien, Y.H., 2013. Effects of feeding frequency and photoperiod on water
quality and crop production in a tilapia-water spinach raft aquaponics system.
Int. Biodeterior. Biodegrad. 85, 693e700. https://doi.org/10.1016/j.ibiod.2013.
03.029.
Love, D.C., Fry, J.P., Genello, L., Hill, E.S., Frederick, J.A., Li, X., Semmens, K., 2014. An
international survey of aquaponics practitioners. PLoS One 9, 1e10. https://doi.
org/10.1371/journal.pone.0102662.
Love, D.C., Fry, J.P., Li, X., Hill, E.S., Genello, L., Semmens, K., Thompson, R.E., 2015a.
Commercial aquaponics production and profitability: findings from an inter-
national survey. Aquaculture 435, 67e74. https://doi.org/10.1016/j.aquaculture.
2014.09.023.
Love, D.C., Uhl, M.S., Genello, L., 2015b. Energy and water use of a small-scale raft
aquaponics system in Baltimore, Maryland, United States. Aquacult. Eng. 68,
19e27. https://doi.org/10.1016/j.aquaeng.2015.07.003.
Mangmang, J.S., Deaker, R., Rogers, G., 2015. Response of lettuce seedlings fertilized
with fish effluent to Azospirillum brasilense inoculation. Biol. Agric. Hortic. 31,
61e71. https://doi.org/10.1080/01448765.2014.972982.
Marques, B., Calado, R., Lillebø, A.I., 2017. New species for the biomitigation of a
super-intensive marine fish farm effluent: combined use of polychaete-assisted
sand filters and halophyte aquaponics. Sci. Total Environ. 599e600, 1922e1928.
https://doi.org/10.1016/j.scitotenv.2017.05.121.
Mashifane, T.B., Moyo, N.A.G., 2014. Acute toxicity of selected heavy metals to
Oreochromis mossambicus fry and fingerlings. Afr. J. Aquat. Sci. 39, 279e285.
https://doi.org/10.2989/16085914.2014.960358.
Maucieri, C., Nicoletto, C., Junge, R., Schmautz, Z., Sambo, P., Borin, M., 2018. Hy-
droponic systems and water management in aquaponics: a review. Ital. J. Agron.
13, 1e11. https://doi.org/10.4081/ija.2017.1012.
Mcmurtry, M.R., Sanders, D.C., Cure, J.D., Hudson, R.G., Haning, B.C., Amand, P.C.S.,
1997. Efficiency of water use of an integrated fish/vegetable co-culture system.
J. World Aquacult. Soc. 28, 420e428. https://doi.org/10.1111/j.1749-7345.1997.
tb00290.x.
Mili

cic, V., Thorarinsdottir, R., Dos Santos, M., Han
ci

c, M.T., 2017. Commercial
aquaponics approaching the European market: to consumers' perceptions of
aquaponics products in Europe. Water 9, 1e22. https://doi.org/10.3390/
w9020080.
Molovan, I., B ala, M., 2015. Analysis of aquaponic organic hydroponics from the
perspective of setting costs and of maintenance on substratum and floating
shelves systems. J. Hortic. For. Biotechnol. 19, 73e76.
Monsees, H., Keitel, J., Paul, M., Kloas, W., Wuertz, S., 2017a. Potential of aquacul-
tural sludge treatment for aquaponics: evaluation of nutrient mobilization
under aerobic and anaerobic conditions. Aquac. Environ. Interact. 9, 9e18.
https://doi.org/10.3354/aei00205.
Monsees, H., Kloas, W., Wuertz, S., 2017b. Decoupled systems on trial: eliminating
bottlenecks to improve aquaponic processes. PLoS One 12, 1e18. https://doi.org/
10.1371/journal.pone.0183056.
Mudahar, M.S., Hignett, T.P., 1985. Energy efficiency in nitrogen fertilizer produc-
tion. Energy Agric. Elsevier Sci. Publ. B.V 4, 159e177. https://doi.org/10.1016/
0167-5826(85)90014-2.
Naegel, L.C.A., 1977. Combined production of fish and plants in recirculating water.
Aquaculture 10, 17e24. https://doi.org/10.1016/0044-8486(77)90029-1.
Nozzi, V., Strofaldi, S., Piquer, I.F., Di Crescenzo, D., Olivotto, I., Carnevali, O., 2016.
Amyloodinum ocellatum in Dicentrarchus labrax: study of infection in salt
water and freshwater aquaponics. Fish Shellfish Immunol. 57, 179e185. https://
doi.org/10.1016/j.fsi.2016.07.036.
 B. Yep, Y. Zheng / Journal of Cleaner Production 228 (2019) 1586e1599
Oelkers, E.H., Valsami-Jones, E., 2008. Phosphate mineral reactivity and global
sustainability. Elements 4, 83e87.
Palm, H.W., Knaus, U., Appelbaum, S., Goddek, S., Strauch, S.M., Vermeulen, T.,
Haïssam Jijakli, M., Kotzen, B., 2018. Towards commercial aquaponics: a review
of systems, designs, scales and nomenclature. Aquacult. Int. 1e30. https://doi.
org/10.1007/s10499-018-0249-z.
Palm, H.W., Seidemann, R., Wehofsky, S., Knaus, U., 2014. Significant factors
affecting the economic sustainability of closed aquaponic systems. Part I: sys-
tem design, chemo-physical parameters and general aspects. AACL Bioflux 7,
20e32.
Pantanella, E., Cardarelli, M., Colla, G., Rea, E., Marcucci, A., 2012. Aquaponics vs.
Hydroponics: production and quality of lettuce crop. Acta Hortic. (Wagening.)
927, 887e894. https://doi.org/10.17660/ActaHortic.2012.927.109.
Pantanella, E., Cardarelli, M., Di Mattia, E., Colla, G., 2015. Aquaponics and food
safety: effects of UV sterilization on total coliforms and lettuce production. Acta
Hortic. (Wagening.) 1062, 71e76. https://doi.org/10.17660/ActaHortic.2015.
1062.8.
Pattillo, D.A., 2017. An overview of aquaponic systems: hydroponic components.
NRAC Tech. Bull. Ser. 19, 1e10.
Radzki, W., Gutierrez Man ~ ero, F.J., Algar, E., Lucas García, J.A., García-Villaraco, A.,
Ramos Solano, B., 2013. Bacterial siderophores efficiently provide iron to iron-
starved tomato plants in hydroponics culture. Antonie van Leeuwenhoek. Int.
J. Gen. Mol. Microbiol. 104, 321e330. https://doi.org/10.1007/s10482-013-9954-
9.
Rakocy, J.E., 2012. Chapter 14: aquaponicseintegrating fish and plant culture. In:
Aquaculture Production System. Wiley, Hoboken, pp. 343e386.
Rakocy, J.E., 2003. Aquaponics d integrating fish and plant culture. In: Aquaculture
Production Systems, pp. 343e386. https://doi.org/10.1002/9781118250105.
ch14.
Rakocy, J.E., Bailey, D.S., Shultz, R.C., Thoman, E.S., 2010. Update on tilapia and
vegetable production in the UVI aquaponic system. In: Proceedings from the
6th International Symposium on Tilapia in Aquaculture, pp. 1e15.
Rakocy, J.E., Masser, M.P., Losordo, T.M., 2006. Recirculating aquaculture tank pro-
duction systems: aquaponics- integrating fish and plant culture. SRAC Publ. -
South. Reg. Aquac. Cent. 16.
Rakocy, J.E., Shultz, R.C., Bailey, D.S., Thoman, E.S., 2004. Aquaponic production of
tilapia and basil: comparing a batch and staggered cropping system. Acta
Hortic. (Wagening.) 648, 63e69. https://doi.org/10.17660/ActaHortic.2004.648.
8.
Resh, H.M., 2012. Hydroponic Food Production: A Definitive Guidebook for the
Advanced Home Gardener and the Commercial Hydroponic Grower. CRC Press,
Boca Raton, FL, USA.
Resh, H.M., 1995. Hydroponic Food Production. Woodbridge Press Publishing
Company, Santa Barbara, California.
Roosta, H.R., 2014. Effects of foliar spray of K on mint, radish, parsley and coriander
plants in aquaponic system. J. Plant Nutr. 37, 2236e2254. https://doi.org/10.
1080/01904167.2014.920385.
Roosta, H.R., Mohsenian, Y., 2012. Effects of foliar spray of different Fe sources on
pepper (Capsicum annum L.) plants in aquaponic system. Sci. Hortic. 146,
182e191. https://doi.org/10.1016/j.scienta.2012.08.018.
Rose, A.L., Waite, T.D., 2002. Kinetic model for FE(II) oxidation in seawater in the
absence and presence of natural organic matter. Environ. Sci. Technol. 36,
433e444. https://doi.org/10.1021/es0109242.
Ru, D., Liu, J., Hu, Z., Zou, Y., Jiang, L., Cheng, X., Lv, Z., 2017. Improvement of
aquaponic performance through micro- and macro-nutrient addition. Environ.
Sci. Pollut. Res. 24, 16328e16335. https://doi.org/10.1007/s11356-017-9273-1.
Rupasinghe, J.W., Kennedy, J.O.S., 2010. Economic benefits of integrating a
hydroponic-lettuce system into a barramundi fish production system. Aquacult.
Econ. Manag. 14, 81e96. https://doi.org/10.1080/13657301003776631.
Rurangwa, E., Verdegem, M.C.J., 2015. Microorganisms in recirculating aquaculture
systems and their management. Rev. Aquacult. 7, 117e130. https://doi.org/10.
1599
1111/raq.12057.
Savidov, N. a., Hutchings, E., Rakocy, J.E., 2007. Fish and plant production in a
recirculating aquaponic system a new approach to sustainable agriculture in
Canada. Acta Hortic. (Wagening.) 742, 209e222. https://doi.org/10.17660/
ActaHortic.2007.742.28.
Schmautz, Z., Graber, A., Jaenicke, S., Goesmann, A., Junge, R., Smits, T.H.M., 2017.
Microbial diversity in different compartments of an aquaponics system. Arch.
Microbiol. 199, 613e620. https://doi.org/10.1007/s00203-016-1334-1.
Schmautz, Z., Loeu, F., Liebisch, F., Graber, A., Mathis, A., Bulc, T.G., Junge, R., 2016.
Tomato productivity and quality in aquaponics: comparison of three hydro-
ponic methods. Water 8, 1e22. https://doi.org/10.3390/w8110533.
Seawright, D.E., Stickney, R.R., Walker, R.B., 1998. Nutrient dynamics in integrated
aquaculture-hydroponics systems. Aquaculture 160, 215e237. https://doi.org/
10.1016/S0044-8486(97)00168-3.
Shiklomanov, I., 1998. World water resources A new appraisal and assessment for
the 21st century. International Hydrological Programme 1e37.
Sikawa, D.C., Yakupitiyage, A., 2010. The hydroponic production of lettuce (Lactuca
sativa L) by using hybrid catfish (Clarias macrocephalus  C. gariepinus) pond
water: potentials and constraints. Agric. Water Manag. 97, 1317e1325. https://
doi.org/10.1016/j.agwat.2010.03.013.
Silva, L., Valdes-Lozano, D., Escalante, E., Gasca-Leyva, E., 2018. Dynamic root
floating technique: an option to reduce electric power consumption in aqua-
ponic systems. J. Clean. Prod. 183, 132e142. https://doi.org/10.1016/j.jclepro.
2018.02.086.
Sonneveld, C., Voogt, W., 2009. Nutrient management in substrate systems. In:
Plant Nutrition of Greenhouse Crops. Springer, Heidelberg, The Netherlands,
pp. 277e312. https://doi.org/10.1007/978-90-481-2532-6.
Timmons, M., Ebling, J., 2010. Recirculating Aquaculture, second ed. (Ithaca NY,
USA).
Tokunaga, K., Tamaru, C., Ako, H., Leung, P., 2015. Economics of small-scale com-
mercial aquaponics in hawai'i. J. World Aquacult. Soc. 46, 20e32. https://doi.
org/10.1111/jwas.12173.
Turcios, A.E., Papenbrock, J., 2014. Sustainable treatment of aquaculture effluents-
What can we learn from the past for the future? Sustain. Times 6, 836e856.
https://doi.org/10.3390/su6020836.
Tyson, R.V., Simonne, E.H., Treadwell, D.D., White, J.M., Simonne, A., 2008. Recon-
ciling pH for ammonia biofiltration and cucumber yield in a recirculating
aquaponic system with perlite biofilters. Hortscience 43, 719e724.
Tyson, R.V., Treadwel, D.D., Simonne, E.H., 2011. Opportunities and challenges to
sustainability in aquaponic systems. HortTechnology 21, 6e13.
Vermeulen, T., Kamstra, A., 2013. The need for systems design for robust aquaponic
systems in the urban environment. In: IS on Soilless Cultivation, pp. 71e78.
https://doi.org/DOI: 10.17660/ActaHortic.2013.1004.6.
Villarroel, M., Alvarin ~ o, J.M.R., Duran, J.M., 2011. Aquaponics: integrating fish
feeding rates and ion waste production for strawberry hydroponics. Spanish J.
Agric. Res. 9, 537. https://doi.org/10.5424/sjar/20110902-181-10.
Wongkiew, S., Hu, Z., Chandran, K., Lee, J.W., Khanal, S.K., 2017a. Nitrogen trans-
formations in aquaponic systems: a review. Aquacult. Eng. 76, 9e19. https://doi.
org/10.1016/j.aquaeng.2017.01.004.
Wongkiew, S., Popp, B.N., Kim, H.J., Khanal, S.K., 2017b. Fate of nitrogen in floating-
raft aquaponic systems using natural abundance nitrogen isotopic composi-
tions. Int. Biodeterior. Biodegrad. 125, 24e32. https://doi.org/10.1016/j.ibiod.
2017.08.006.
Zou, Y., Hu, Z., Zhang, J., Xie, H., Guimbaud, C., Fang, Y., 2016a. Effects of pH on
nitrogen transformations in media-based aquaponics. Bioresour. Technol. 210,
81e87. https://doi.org/10.1016/j.biortech.2015.12.079.
Zou, Y., Hu, Z., Zhang, J., Xie, H., Liang, S., Wang, J., Yan, R., 2016b. Attempts to
improve nitrogen utilization efficiency of aquaponics through nitrifies addition
and filler gradation. Environ. Sci. Pollut. Res. 23, 6671e6679. https://doi.org/10.
1007/s11356-015-5898-0.