Journal PSTR 0000076

PLOS SUSTAINABILITY AND TRANSFORMATION
RESEARCH ARTICLE
A nature-based solutions approach to

managing shrimp aquaculture effluent
Garrett M. Goto ID1*, Emily Corwin1, Alexander Farthing2, Anisa Rilla Lubis2, Dane
H. Klinger1
1 Conservation International, Arlington, Virginia, United States of America, 2 Alune Aqua Ltd., Cork, Ireland
* [email protected]
a1111111111 Abstract
a1111111111
a1111111111 While coastal habitat conversion was a primary environmental concern in Asia for the mostly
a1111111111 extensive shrimp aquaculture sector in previous decades, the transition towards intensive
a1111111111 production is creating new environmental risks, primarily water quality impacts from nutri-
ent-rich effluent. There is a need to compare the performance of conventional and Nature-
based Solution (NbS) effluent treatment options given the increasing nutrient loads from
more intensive aquaculture and historic loss of ecosystem services from mangrove defores-
OPEN ACCESS tation. This study evaluates the potential for common and emerging effluent treatment sys-
Citation: Goto GM, Corwin E, Farthing A, Lubis AR, tems to address total nitrogen and total phosphorus effluent from shrimp farms across a
Klinger DH (2023) A nature-based solutions spectrum of production intensities. Nutrient waste loading for four stocking density scenarios
approach to managing shrimp aquaculture effluent.
(7PLm-2, 20PLm-2, 75PLm-2, and 120PLm-2) are estimated to compare the treatment effi-
PLOS Sustain Transform 2(8): e0000076. https://
doi.org/10.1371/journal.pstr.0000076 ciency, economic feasibility, spatial requirements, and ecosystem service provision of con-
ventional and NbS effluent treatment systems. We use secondary data to assess effluent
Editor: Lian Pin Koh, National University of
Singapore, SINGAPORE treatment systems applicable for shrimp aquaculture in Asia. Findings provide the concep-
tual framework for comparing the characteristics and tradeoffs of aquaculture effluent treat-
Received: August 15, 2022
ment systems. Constructed mangrove wetlands are an NbS approach that can meet the
Accepted: July 20, 2023
intensification needs of aquaculture producers and reduce negative impacts from aquacul-
Published: August 30, 2023 ture effluent at competitive costs, while also providing ecosystem service co-benefits.
Copyright: © 2023 Goto et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original Author summary
author and source are credited.
Shrimp aquaculture expansion has been a primary driver of mangrove deforestation and
Data Availability Statement: All data used is noted degradation globally. Although deforestation rates have slowed considerably in the last
in the manuscript and S1 Text (Supplementary two decades, the loss of these critical ecosystems leaves coastal communities vulnerable to
Methods).
climate change risks, like sea level rise and increasing storm surge intensity. Concurrently,
Funding: GMG, EC, AF, ARL, and DHK were the shrimp aquaculture sector has been trending towards more intensive production,
supported by a grant from The David and Lucile resulting in higher production volumes and the concentrated release of nutrient-rich
Packard Foundation (Grant #2020-71358), and
effluent into aquatic ecosystems. These imminent environmental threats from shrimp
GMG, EC, and DHK were supported by a grant
from Foundation of Success (“Conservation at aquaculture motivate our study focused on common and emerging effluent management
Scale”). The funders had no role in study design, approaches. We model four shrimp production intensity scenarios to estimate nutrient
data collection and analysis, decision to publish, or waste loads and use those waste loads as inputs to compare seven conventional and
preparation of the manuscript.
PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 1 / 32

PLOS SUSTAINABILITY AND TRANSFORMATION A nature-based Solutions approach to managing shrimp aquaculture effluent
Competing interests: I have read the journal’s

policy and the authors of this manuscript have the Nature-based Solution (NbS) effluent treatment systems. Effluent treatment systems are
following competing interests: D.H.K. is a member evaluated based on removal rate efficiencies, equivalent annual costs per kg harvested,
of the Technical Advisory Group for the
spatial footprint requirements, and ecosystem service provision. Our results suggest that
Aquaculture Stewardship Council and a member of
the Aquaculture Technical Advisory Committee of
constructed mangrove treatment wetlands, a type of NbS approach, are not only an eco-
Monterey Bay Aquarium’s Seafood Watch nomically viable option for effluent management compared to more conventional
Program. The other authors have declared that no approaches, such as settling ponds, but can also provide additional ecosystem services.
competing interests exist. Our study demonstrates how an NbS approach can be applied to shrimp aquaculture
while accommodating commercial production needs and trends towards intensification.
Introduction
The substantial growth of global shrimp aquaculture has often come at the expense of coastal
ecosystems, such as mangrove forests, which have been cleared to create new shrimp ponds.
Global shrimp aquaculture production has increased by 10,000% in 40 years, from an esti-
mated 74,000 metric tons (t) in 1980 to 7.43 million t in 2020 [1]. The majority of which, 83%
(6.13 million t), originated from Asia, with China alone accounting for 2.57 million t and
other top producing Asian countries (e.g., Viet Nam, India, Indonesia, Thailand, Bangladesh,
Myanmar, Philippines, and Malaysia) contributing a combined 3.46 million t over the same
time period [1].
Addressing emerging challenges that come with such growth, such as pollution and
degraded water quality linked with intensification, while also rectifying the damage and eco-
system services lost from mangrove deforestation, will require new strategies to align environ-
mental and economic incentives. Approaches that utilize Nature-based Solutions (NbS), in
which the designed function of the system (e.g. nutrient effluent mitigation) can also provide
ecosystem benefits, show promise in that they employ, “actions to protect, sustainably manage
and restore natural or modified ecosystems that [also] address societal challenges effectively and
adaptively, simultaneously providing human well-being and biodiversity benefits” [2]. The
United Nation’s Environmental Programme asserts that NbS are a restorative and cost-effec-
tive climate tool [3], but their viability and potential applications in aquaculture systems are
nascent and far less understood [4,5].
Conversely, conventional treatment systems in this study are those that are manufactured
or built, are static, and cannot adapt as environmental conditions change, nor are they able to
recover or grow back after environmental or structural disturbances. These types of systems
can be categorized as “gray infrastructure”, which have a specific design life, during which they
require appropriate maintenance and operation and after which they can no longer be
expected to provide the designed service [6].
NbS are gaining support for more conventional applications, but a lack of bankable projects
and general unfamiliarity for these types of solutions have limited their use [7]. Conventional
built structures, like manufactured commercial filters housed in buildings, have a finite life-
span and limited resilience to a rapidly changing coastal environment. Structures that can
incorporate climate-resilience strategies are likely to reduce damages from environmental dis-
turbances and increase longevity [8]. Hybrid approaches, such as constructed treatment wet-
lands, that can integrate conventional engineering techniques with NbS, may be a strategy that
minimizes the limitations of using either approach individually [6]. This type of integration of
NbS may benefit coastal shrimp aquaculture and should be explored further.
Shrimp are commonly farmed in ponds and tanks under a range of production intensities,
broadly categorized as extensive, semi-intensive, intensive, and super-intensive. These

intensities are typically defined by multiple, linked metrics, including stocking density (indi-
vidual post-larvae (PL) shrimp per m2 per cycle) and harvested yield (t per hectare (ha) per
cycle or per year) [9]. The gradations between these categories of production intensity are not
universally defined and vary by farming region and across time [10–14]. Pacific whiteleg
shrimp (Litopenaeus vannamei) are typically preferred for more intensive production systems
[15] but are grown across a spectrum of intensities characterized by different levels of manage-
ment, stocking densities, and yields (Table 1). Extensive production utilizes few to no inputs
(i.e., relying mostly on natural productivity to provide seed, feed, and water treatment) while
intensive and super-intensive production are entirely dependent on external inputs (i.e., farm-
ers must provide increasing amounts of seed, feed, and water treatment) [16]. Increasing pro-
duction intensity requires financial investments and additional technical capacity, both of
which are often barriers for farmers to intensify from low (extensive) stocking density upwards
to medium (semi-intensive), high (intensive), and very high (super-intensive) stocking densi-
ties [15].
While habitat conversion was the primary environmental concern for the mostly extensive
shrimp aquaculture sector in previous decades [18–21], the shift to more intensive production
creates new environmental risks, such as water quality impacts from nutrient-rich effluent
(Fig 1). As production intensifies, supplemental feed is required to meet the metabolic require-
ments of the shrimp. Excess nutrients that are not utilized to create shrimp biomass, such as
Table 1. Whiteleg shrimp (Litopenaeus vannamei) production intensities and characteristics.

Extensive Semi-Intensive Intensive Super-Intensive
Water Quality Limited to no water quality management Use of probiotics, fertilizers, and other High use of inputs, some Precision technology and
Management interventions, passive tidal flushing. inputs. Increased daily water exchange have pretreatment ponds. high use of inputs.
with pumping.
Feed Manufactured pellet feed rarely used, dependent Mostly manufactured pelleted feed or Dependent on Dependent on high-
on natural productivity and/or fertilizers to farm-made feeds. manufactured pellets. quality manufactured
stimulate natural productivity. pellets.
Aerators None Few Aerators essential Many aerators are
essential
Stocking Density
(PL m-2)
Indonesia [10] 1 to 10 – 50 to 150 > 200
Indonesia [13] 4 to 10 10 to 30 60 to 300 300 to 750
Viet Nam [15] < 10 10 to 29 > 30 –
Viet Nam [11] – 26 to 31 66 73
Thailand [11] – 62.51 82 99
Production Yield
(t ha-1 yr-1)
Viet Nam [15] < 0.70 < 3.5 > 3.5 –
Viet Nam [11] – 0.27 to 3.5 7 11.7
Thailand [11] – 1.3 to 3.5 7 13.6
Indonesia [10] <5 – 5 to 30 30 to 80
Not country- 0.25 to 0.5 1 to 3 4 to 20 >20
specific [17]
Not country- <1 2 to 20 20 to 200 > 200
specific [12]
1
The stocking density for medium-intensity production from this study is higher compared to other sources but meets the other criteria for semi-intensive production.
This can be a result of feeding rate, harvest weight of the shrimp, survivability or other factors.
https://doi.org/10.1371/journal.pstr.0000076.t001

Fig 1. The spectrum of production intensities, expressed as yield in metric tons (t) per ha per cycle and stocking density post-larvae (PL) per m2
per cycle, associated with four categories of shrimp aquaculture production. Habitat conversion risk per t is relative to the spatial footprint required
by each production category. Pollution risk per hectare is relative to the amounts of effluent discharged from production systems. Photo credits from
top to bottom: a) Super-intensive indoor shrimp farm in Nha Mat, Bac Lieu, Vietnam. Courtesy of Viet-Uc Seafood Corporation. b) Intensive cement-
lined shrimp farm in East Java, Indonesia. c) Semi-intensive earthen shrimp ponds in Guayas, Ecuador. d) Extensive shrimp pond in Guanacaste, Costa
Rica.
https://doi.org/10.1371/journal.pstr.0000076.g001
uneaten feed or those excreted by the shrimp, can pose an environmental risk when loads are
discharged into adjacent coastal waterways without adequate treatment [22]. Feed can contrib-
ute 60% to 96% of total nitrogen (TN) and 12% to 95% of total phosphorus (TP) in aquaculture
effluents [23–29]. Dissolved nutrients, like an excess of reactive nitrogen, impact the health of
coastal ecosystems by disrupting nutrient dynamics, especially in areas with low mixing rates
or densely concentrated production regions [30–35]. Settleable solids (SS), a measure of mate-
rials that settle from solution in an hour, and total suspended solids (TSS), the weight of filter-
able solid material in the water column, are together the amount of recoverable particulate
matter from effluent through settling or filtration [36], which can impact benthic environ-
ments if discharged. Dissolved and particulate effluents from aquaculture have negatively
impacted seagrass beds [37], contributed to harmful algal blooms [38], and increased turbidity
and sedimentation [39], which have smothered coral reefs [40]. The increased loading of nutri-
ent effluents per unit area of production associated with intensification amplifies the potential
for untreated waste to degrade surrounding water bodies and ecosystems [22], such as through
acidification, eutrophication, and ecotoxicological impacts [16,41].
The landscape of shrimp aquaculture production is changing to keep up with growing
demand for seafood, characterized by increasing production intensification trends [21,42,43]
(see [43] for a history of shrimp aquaculture). For example, average production intensity
across all of Indonesia, one of the largest shrimp producing countries in Asia [44], increased
from 0.17 t ha-1 to 1.49 t ha-1 between 1986 and 2019 (calculated as production in t divided by
shrimp pond area [45,46]). Meanwhile, the real price of farmed shrimp has decreased on aver-
age for the last several decades [47], meaning farmers must reduce production costs to remain
profitable [43]. Intensification can achieve such cost reductions on a per unit basis [48], largely

through improved resource efficiency at the farm level [17]. Increasing production intensity
per unit area creates an opportunity to increase overall production yield without expanding
direct land requirements [49]. There is an estimated 2.1 million ha of shrimp ponds in produc-
tion, however the use of high intensity production could meet current demand with just under
43,000 ha, or 2% of today’s spatial footprint [50].
Shrimp aquaculture production has seen significant growth in recent decades, but innova-
tive strategies to address nutrient waste from increasingly intensive systems are lagging [51].
Previous studies have evaluated aquaculture effluents systems individually [25,52–60] or com-
pared the general characteristics of systems [51,61], but there is a need to understand system
tradeoffs and attributes using uniform inputs. Often, nutrient removal is the primary, or only,
characteristic evaluated, but economic and spatial constraints also play a role in farm decision
making. Given rapidly changing coastal climate and marine conditions, the shrimp aquacul-
ture sector should consider systems that provide ecosystem services, especially those that can
improve coastal adaptation and resilience to natural disturbances [4]. As global demand for
shrimp drives more intensive production, and climate change impacts increase in their inten-
sity, there is an opportunity to address both nutrient effluent wastes and climate resilience
through the introduction of NbS into shrimp aquaculture effluent treatments.
This study evaluates the potential of conventional and NbS effluent treatment systems for
addressing TN and TP from shrimp farm effluent across a spectrum of production intensities.
We use secondary data collected from literature review to model the effluent treatment
requirements of systems that are prevalent in Asia for shrimp aquaculture. Nutrient waste
loading for a range of stocking densities is estimated to compare the treatment efficiency and
economic feasibility of conventional and NbS effluent treatment systems for shrimp aquacul-
ture. Effluent treatment systems that convey benefits to farmers and the environment are then
highlighted. Results from this study provide a comparison of pollutant removal efficiencies,
economic considerations, spatial requirements, ecosystem service provision, and suggested
areas of research. These findings provide the conceptual framework for comparing the charac-
teristics and tradeoffs of shrimp aquaculture effluent treatments.
Materials and methods

Research approach
Due to a paucity of publicly available farm-level primary data, this study models shrimp aqua-
culture effluent waste for four stocking densities based on average L. vannamei production
parameters [17] and nutrient loading [34] with a focus on production system trends in Asia.
The four scenarios include stocking densities of 7 PLm-2, 20 PLm-2, 75 PLm-2, and 120 PLm-2
to capture a range of production intensities. Super-intensive ponds systems (e.g., stocking den-
sities of 125 to 252PLm-2) have been reported in Indonesia [62] but are less common and,
thus, such a scenario was not included. The modelled TN and TP loads from the four stocking
density scenarios are used as inputs for each of the evaluated effluent treatment systems to esti-
mate their pollutant removal effectiveness, farm-level economics, spatial requirements, and
ecosystem service provision (Fig 2). Data were drawn from a review of academic, industry,
and popular press literature.
Evaluated treatment systems

Effluent treatment systems are categorized as either conventional or NbS if the system is able
to “protect, sustainably manage, or restore natural or modified ecosystems” [2] (Table 2). Com-
mon and emerging effluent treatment systems within both categories were chosen to show a
range of potential approaches that have proven some commercial viability. Settling ponds or

Fig 2. Conceptual analysis diagram for the study. Stocking densities of 7 PLm-2, 20 PLm-2, 75 PLm-2, and 120 PLm-2 represent a range of common
production intensities in Asia. Effluent, modelled as TN and TP, from each of the stocking densities are used as inputs for conventional and NbS
treatment systems. Performance criteria for each treatment system and stocking density combination was evaluated based on water quality, economic,
and spatial requirement criterium and ecosystem service provision.
https://doi.org/10.1371/journal.pstr.0000076.g002
basins are the most widely used treatment system, and are a requirement for international cer-
tifications [63,64]. Commercial filters are typically only used for high- and super-intensive
shrimp production [65], while woodchip bioreactors are emerging systems in aquaculture but
have proven application in other sectors [66]. Silvoaquaculture, also referred to as mixed man-
grove-shrimp farming, is commonly practiced in Vietnam and parts of Indonesia [59]. Biofil-
tration, or integrated multi-tropic aquaculture (IMTA), as an effluent mitigation approach has
been researched [60,67,68], but is limited in its commercial application. The use of existing
mangrove forests to treat aquaculture effluent is often a post facto decision, where the location
and use of the forest is opportunistic, rather than designed [56,69], which poses significant
environmental risks [70]. Constructed treatment wetlands can provide many of the same envi-
ronmental and effluent treatment benefits of existing mangroves, but in a deliberate and
designed way for appropriate nutrient loads [71]. Apart from silvoaquaculture (which can
include the integration of mangroves within the production pond) the selected treatment sys-
tems focus on post-production effluent management, noting that there are a wide range of
farm-level practices (e.g., feeding regimes, biofloc, etc.) that can influence water quality but are
not within the scope of this study. Table 2 provides a brief description of each system, its mech-
anism to treat effluent, and prevalence of use in shrimp aquaculture. Additional information
and conceptual diagrams provided in Table A in S1 Text.
Data collection and analysis

Effluent composition. Four production intensities, based on stocking densities of
7 PLm-2, 20 PLm-2, 75 PLm-2, and 120 PLm-2, were chosen to represent a spectrum of common

Table 2. Treatment systems categorized by solution type (i.e., conventional or NbS) and their characteristics.
Treatment System Solution Type Description Mechanism Application References
Commercial Filters Conventional Commercial filtration systems use Microbial biofiltration converts Widely used in land-based [54,72–74]
mechanical filters to remove solid dissolved nitrogen wastes through Recirculating Aquaculture
wastes through the physical the breakdown of unionized Systems (RAS) but are generally
separation of particle sizes and ammonia to nitrite and then the cost-prohibitive for pond-based
biofilters to convert toxic mineralization of nitrite into systems.
nitrogenous waste into non-toxic nitrate by autotrophic bacteria that
nitrate via microbial activity. colonize a bio-media substrate in a
filter, such as a fluidized-sand
biofilter [72] and moving bed
biofilm reactors.
Woodchip Conventional Woodchip bioreactors direct Wood media, often wood chips, Have been applied in other [55,75–78]
Bioreactors effluent through designated carbon- enhance the passive treatment of industries (e.g., to treat
filled trenches that host denitrifying nitrate-nitrogen by hosting agricultural runoff) but are rare in
bacteria. microbial biomass [66]. the aquaculture sector.
Settling Ponds Conventional Settling ponds, or sedimentation The physical process of Typical post-production [25,52,80,81]
basins, are designated areas of a sedimentation is defined by Stoke’s treatment systems for pond
farm that accept effluent discharge Law [79], which calculates the aquaculture due to their simple
from production ponds throughout settling velocities of particles design and ease of use.
the production cycle and during suspended in the water, primarily
harvest. as a function of particle size,
density, water temperature, and
flow rate [80].
Biofiltration Nature-Based Biofiltration in this context involves IMTA has a broad range of Gaining popularity in general, but [82–85]
(Integrated Multi- Solution nitrogen removal by shellfish when applications but can be defined as its application for biofiltration to
Trophic Aquaculture, incorporated into shellfish biomass growing species from two or more treat effluent is still experimental.
IMTA) (e.g tissue and shells) and removed trophic levels in the same
during harvest [82]. production area where the wastes
from one species provides the
nutrient inputs for another species
[83, 84].
Silvoaquaculture Nature-Based Silvoaquaculture integrates Low stocking densities in these Widely used in Vietnam with [59,86,87]
Solution mangrove forestry and the systems usually require few limited use in other production
cultivation of aquatic species [59]. additional inputs, meaning geographies.
These systems are primarily differences in water quality of
extensive but can be semi-intensive production ponds and surrounding
when supplemented with hatchery areas are not significantly different.
grown seed. Water quality changes with the
addition of feed and can be
adversely affected by decomposing
leaf litter [59].
Constructed Nature-Based Constructed wetlands can use either, Constructed wetlands treat There are a wide range of [71,89–91]
Treatment Wetlands Solution or a combination of, surface and wastewater from multiple sources wastewater applications but their
subsurface hydrologic flow to [88] where nutrient removal occurs use in the tropics, and with
mitigate nutrients and accumulate as a result of biotic and abiotic coastal species such as mangroves,
solids through the use of processes through substrate media, have largely been focused on field
geomorphic design and vegetation vegetation (macrophytes), diverse experiments and trials.
[71]. microbial communities, and other
chemical processes.
Existing Mangrove Nature-Based Mangrove forests for wastewater The nutrient remediation processes Studies have evaluated the [56,69,93]
Forests Solution treatment utilize existing, matured in mangrove wetlands include impacts of aquaculture effluent on
vegetation and a passive hydrology sedimentation, decomposition of mangrove forests, but few have
design. organic matter, assimilation of evaluated them as an effluent
nutrients by plants, bacteria management tool.
nitrification and dentification, and
ion absorption by soil compounds
[92].

production scenarios to model TN and TP effluent waste loads. Generalized production

parameters for L. vannamei were used to estimate yield, Y (t ha-1 yr-1) (Eq 1) and feed require-
ments (Eq 1) [17].
1
Y ¼ ð½ðA � D � S � WÞ � 1000 � 1000 1 � � C ð1Þ
Where A = pond area (m2), D = stocking density (PL m-2), S = survival (%), W = shrimp
weight at harvest (g), and C = harvest cycles (# yr-1). Total feed requirements, F (t yr-1), can be
estimated by multiplying yield by an average feed conversion ratio (FCR) as described in Eq 2.
F ¼ Y � FCR ð2Þ
Effluent loads for TN (Eq 3) and TP (Eq 4) were estimated assuming an FCR of 1.5 and the
difference of nitrogen and phosphorus in feed compared to the weight of harvested biomass
[34].
h � � i
Nw ¼ ðFCRÞ Nf Nc � 1000 ð3Þ
h � � i
Pw ¼ ðFCRÞ Pf Pc � 1000 ð4Þ
Where Nw and Pw are nitrogen and phosphorus waste loads (kg t-1 of cultured species), Nf and
Pf are decimal fractions of nitrogen and phosphorus in the feed, and Nc and Pc are the decimal
fractions of nitrogen and phosphorus in the live weight of harvested shrimp biomass. Produc-
tion parameters and assumptions are provided in Table 3. Calculated values for the effluent
waste load of TN and TP were used as inputs for each treatment system. Assumptions and
detailed calculations provided in S1 Text.
Table 3. Production parameters and assumptions for modelled scenarios [17,34].

Parameter Unit Modelled Scenarios 75PLm-2 120PLm-2
-2 -2
7PLm 20PLm
Production Pond Area (this study) ha 1 1 1 1
Production Pond Depth (this study) m 1 1 1 1
Stocking Density (this study) PLm-2 7 20 75 120
Survival % 60 60 70 70
Shrimp Weight at Harvest g 18 18 16 16
Crop Duration days/crop 110 110 80 80
Harvest Cycles #yr-1 2.2 2.2 2.5 2.5
FCR kg kg-1 1.5 1.5 1.5 1.5
Average percentage of nitrogen in whiteleg shrimp % 2.86 2.86 2.86 2.86
Average percentage of phosphorus in whiteleg shrimp % 0.32 0.32 0.32 0.32
Air-dry concentration of phosphorus in grower feeds % 5.33 5.33 5.33 5.33
Air-dry concentration of nitrogen in grower feeds % 1.12 1.12 1.12 1.12
Nitrogen waste load kg t-1 37 37 37 37
-1
Phosphorus waste load kg t 11.7 11.7 11.7 11.7
Production Yield t ha-1 yr-1 1.66 4.75 21 33.6
Feed Requirement t yr-1 2.5 7.13 31.5 50.4
Total Nitrogen, TN (this study) kgN ha-1 yr-1 62 176 777 1,243
Total Phosphorus, TP (this study) kgP ha-1 yr-1 19 56 246 393

Water quality criteria. Nutrient and suspended solids removal rates, expressed as a per-
cent decrease from influent concentrations, are reported as minimum and maximum values
based on a literature review. Removal rates can vary across and within treatment types due to
biotic and abiotic factors and as a function of hydraulic residence time, or how long the efflu-
ent is undergoing the decomposition processes. Commercial filters target the removal of
total ammonia nitrogen through an effective nitrification process [54], which resulted in
reporting of total ammonia nitrogen removal rates being more common than TN in the liter-
ature. TSS was also included as a key indicator of water quality improvement, although
reporting on TSS in the literature was less common than for TN and TP. This study assigns
pollution reduction thresholds of at least 40% for TN and TP, and at least 70% reduction for
TSS based on Low Impact Development and Best Management Practice approaches [94], but
actual biophysical thresholds will depend on the conditions and assimilative capacity of the
receiving water body.
Aquaculture certification standards, such as those developed by the Aquaculture Steward-
ship Council (ASC) and Global Seafood Alliance’s Best Aquaculture Practices (BAP), set efflu-
ent pollution limits and require farm-level management practices to decrease the risk of
eutrophication in receiving water bodies [63, 64]. These certification bodies set effluent limits
with allowances of nutrients above that of receiving bodies, recognizing the difficulty for farm-
ers to return discharged wastewater to ambient conditions. The impact of such an effluent
allowance will differ depending on the conditions of the receiving water body, and thus, certifi-
cation standards require compliance with a comprehensive list of precautionary water quality
parameters and management practices to limit cumulative impacts.
The ASC shrimp standard limits annual effluent to 25.2kgTN and 3.9kgTP for L. vannamei
on a per t of harvested shrimp basis (Criterion 7.5.1 and 7.5.2) [63]. Conversely, the BAP stan-
dard sets effluent concentration limits of less than 5 mg/L total ammonia nitrogen and less
than 0.5 mg/L soluble phosphorus (BAP, Appendix B) or compliance with other effluent crite-
ria that can demonstrate limited negative impacts to receiving water bodies (Pillar 3.C. 3.3.2–
6) [64]. Mass loading for nitrogen and phosphorus are required to be recorded by auditors
(Pillar 3.B. 3.1), but only provisional targets have been set at 15kg total ammonia nitrogen t-1
and 1kg soluble phosphorus t-1 (BAP, Appendix A). In addition to nitrogen and phosphorus
criteria, both ASC and BAP include guidance for other water quality and monitoring criteria
to reduce negative impacts on receiving water bodies, such as suspended solids thresholds, lim-
iting changes to dissolved oxygen, and biochemical oxygen demand. Effluent concentrations,
nutrient loads, and total discharge volume–during the production cycle and at pulse events,
such as harvest–are all critical aspects for a comprehensive understanding of effluent
management.
Economic criteria. Capital costs and annual operating costs were collected from literature
and expert inputs with costs adjusted for inflation to USD2021. Capital costs include a treat-
ment-specific lifetime depreciation on items such as hardware and infrastructure, which are
assumed to be 10 years for earthen settling ponds, commercial filters, woodchip bioreactors
[55], and IMTA [95,96]. HDPE-lined settling ponds can have shorter lifespans and increased
operating costs, compared to earthen ponds, if liners get punctured, torn, or degraded but
could be considerably longer with proper maintenance. The effective lifespans for NbS systems
are substantially longer. For example, constructed wetlands were conservatively estimated to
last 20 years [97] but commonly last up to 30 years [71]. Lifespans for silvoaquaculture and
existing mangroves are estimated to be 25 and 50 years, respectively [98,99].
An equivalent annual cost (EAC) for each production scenario within each treatment sys-
tem was used to compare the cost-effectiveness across treatment systems with unequal life-
spans, which is described by the ratio of its net present value to an annuity factor [100]. The

EAC is described in (Eq 5) as:

� 1
EAC ¼ NPV AN; k ð5Þ
Where k = the discount rate, here assumed to be 11.73% for crustacean aquaculture in develop-
ing countries [101], N = the treatment-specific economic lifespan of the asset in years, and
AN, k = the present annuity factor. The annuity factor can be calculated as (Eq 6):
N ��
AN;k ¼ 1 1∗ð1 þ kÞ k 1 ð6Þ
Simply, the initial capital expenses for the asset are divided by the annuity factor and then
added to the expected annual operating costs. Calculated EAC values were then divided by the
estimated shrimp yield in kg to standardize outputs for each production scenario (See Table B
in S1 Text for complete outputs). This model assumes a break-even earnings before interest
and taxes (EBIT) margin of 16% [13]. Using a market price of USD 4.47 per kg [102], a value
of USD 0.18 per kg (4% of EBIT) was selected as the threshold EAC per kg of shrimp, allowing
for an EBIT margin of 12%.
Spatial criteria. Nutrient remediation capacities, typically estimated in terms of mass per
unit area per unit time, were collected through literature review for each of the treatment sys-
tems. Nutrient loading rates in Table 3 were used as inputs to determine the total area required
for each of the modelled scenarios. Spatial requirements for constructed treatment wetlands
used a first-order plug flow kinetic model [58], which required an estimation of influent nutri-
ent concentrations (i.e., into the treatment system) based on total nutrient load, daily water
exchange, and pond volumes (detailed calculations in S1 Text—Supplementary Methods). The
spatial footprint requirements ranged widely across treatment systems and have been reported
as the area, in square meters, proportional to 1 ha of shrimp production pond (i.e., 1,000m2 =
0.1ha:1ha and 25,000m2 = 2.5ha:1ha treatment area to pond ratio). Commercial filters were
only evaluated at the 120 PLm-2 scenario due to the technical and economic requirements of
those systems. Silvoaquaculture is defined by extensive culture and was only evaluated for the
7 PLm-2 scenario. Treatment systems were categorized as above or below a threshold of 0.6ha
based on the area required for a generic sedimentation basin with a hydraulic retention time of
6 hours [52,103]. The hydraulic retention time allows course and medium solids to settle and
is calculated as basin volume divided by the incoming flow rate but does not factor in nutrient
loads or concentrations. Assuming a basin depth of 1m, and that maximum effluent inflow
occurs during harvest over a 10-hour period at a rate of 1,000 m3 hr-1, the calculated basin area
would require 0.6ha.
Ecosystem services. Environmental and social benefits delivered by treatment systems
beyond their intended water quality improvements are captured as ecosystem services. Ratings
for provisioning services, regulating services, cultural services, and supporting services under
different wetland ecosystem types were collected from Ramsar’s Global Wetland Outlook
2018, Table 2.7 [104,105]. Ratings for several of the evaluated wetland ecosystems were directly
transferable to the treatment systems in the study (i.e., settling ponds = “waste ponds”, existing
mangrove forest = “Mangrove”, biofiltration = “Shellfish Reef”), while assigning hybrid ratings
for treatment systems not directly transferable (i.e., silvoaquaculture = “Mangroves” and
“Aqua Ponds” and constructed treatment wetlands = “Mangrove” and “Salt Marsh”). Com-
mercial filters and woodchip bioreactors are treatment systems that do not provide ecosystem
services. ‘High’, ‘Medium’, and ‘Low’ ratings given in the Global Wetland Outlook table were
assigned scores of 3, 2, and 1, based on each systems’ ability to deliver on specified ecosystem
services, respectively (ratings of ‘Not known’ and ‘Not applicable’ given scores of zero). Provi-
sioning services and regulating services had five sub-categories with a possible score of 15

each, while cultural services and supporting services each had four sub-categories with a
potential score of 12 each. Scores for each treatment system and across service types were
summed and their cumulative scores assigned to one of three equal bins (‘High’ = 37 to 54,
‘Medium’ = 19 to 36, ‘Low’ = 0 to 18) or ‘NA’ categories. Treatment systems within the ‘Low’
or ‘NA’ bins were categorized as below the threshold to deliver ecosystem services. Tabulated
scores for all ecosystem services in Table C in S1 Text.
Normalization and aggregation of performance indicators. Overall treatment system
performance for each production intensity scenario was compared by normalizing values
within specific indicators (e.g., TN, TP, TSS, and Ecosystem Services) where higher values
indicated preferred directionality (Eq 7).
1
Zi ¼ Xi Xmax ð7Þ
Where Zi = the normalized indicator value, Xi = the actual indicator value expressed numeri-
cally (e.g., 46% = 0.46), and Xmax = the maximum value expressed numerically of all values
within the indicator category. For the economic criteria and spatial requirement criteria,
where the preferred directionality would be to have lower values, normalizing values included
taking the absolute value of one minus Xi Xmax-1 (Eq 8).
Zi ¼ j1 ðXi Xmax 1 Þj ð8Þ
These normalized values for each treatment system’s performance criteria indicated that
lower values have lower performance, and that higher values achieve higher performance.
With normalized scores being a numerical vector between 0 to 1.00, a color gradient was
applied to emphasize relative scoring for the evaluated indicator under each scenario. Each
performance indicator (e.g., TN, TP, TSS, EAC, m2, and Ecosystem Services) was weighted
equally and multiplied by its normalized score to determine an aggregate indicator for the
treatment system-production scenario combinations. However, in practice, the weights for
specific criteria would be different depending on the location, farmer, production system, or
other factors. This wide diversity of potential preferences suggests that no single combination
of weighting performance indicators would be able to adequately characterize shrimp aquacul-
ture in Asia. Thus, assigning equal weights to all the performance criteria may not accurately
reflect the relative importance of each indicator as this would be context-dependent and vary
by stakeholder preferences. Treatment systems were then ranked by their additive aggregation
indicators e.g., the sum of their normalized scores with equal weights. Threshold values for
each criterion were also normalized and ranked by their aggregation indicators.
Study limitations. A lack of available farm-level effluent data from commercial opera-
tions, especially from more intensive production systems, was a major barrier for this study.
Reports of effluent water quality data from commercial shrimp farms were more prevalent in
older studies and at lower production intensities. Due to the wide variety of potential nutrient
inputs and pond-level management practices across geographies, this study utilized hypotheti-
cal scenarios under uniform conditions to evaluate treatment systems. Audit reports on water
quality are available for ASC certified farms globally, requiring reports on kgN, kgP, and settle-
able solids. While informative, these reported effluent loads are those that are being discharged
into surrounding waterways and have already undergone some level of effluent treatment and
water quality management to achieve ASC’s effluent standards. Additionally, predicting TSS
was sparse and only found in one incidence, where a “rule of thumb” suggested that suspended
solids could be estimated using 25% of the fed quantity of feed [106]. Overall, reporting on
TSS was less common than for TN and TP in literature. Improved monitoring, data collection,

and transparency of current farm-level effluent loading would help to inform management
practices that benefit the environmental sustainability of the sector.
Results
Estimated nutrient loading
Modelled nutrient waste loading scenarios for 7 PLm-2, 20 PLm-2, and 75 PLm-2 fell within
ranges observed in literature, although reported values of TN and TP effluent per unit area (kg
ha-1 yr-1) and per t of shrimp varied considerably across studies (Table 4). Higher stocking
densities of 125 PLm-2 and 252 PLm-2 [62], and up to 750, 1000, and 1200 PLm-2 [107] were
documented in Indonesia, but these studies did not record nutrient effluent loads. The results
from Table 4 highlight the wide range of effluent loads collected from different production sys-
tems and under varying management regimes. As production intensifies, total nutrient dis-
charge (e.g., kgN ha-1 yr-1) would be expected to increase, while nutrient discharge per unit
weight of shrimp (e.g., TN kg-1) would generally decrease. While these trends can loosely be
observed, there are many cases reported in the literature where values are far from the antici-
pated range. These findings further emphasize the complexity of aquaculture effluents under
real-world conditions.
Treatment system performance

This analysis provides a preliminary comparison of shrimp aquaculture effluent treatment sys-
tems across a spectrum of production intensities (Table 5). Ranges of pollution removal col-
lected from literature, expressed as a decrease from initial condition, varied widely within each
treatment system and across system types. Constructed mangrove wetlands and existing man-
grove forests, types of NbS systems, showed cost-competitiveness with settling ponds based on
EAC kg-1 values. While NbS systems require much larger spatial footprints, especially at higher
production intensities, these areas also provide additional ecosystem services beyond their
intended water quality improvements. Target thresholds for each criterion were identified to
help define the relative performance under the various scenarios. Although actual pollutant
removal would be highly dependent on farm-level design and operation of effluent treatment
systems, the economic and environmental results across the production intensity scenarios
suggest that NbS can be a viable aquaculture effluent solution.
Water quality criteria

Nutrient and sediment removal rates varied widely, and no system was found to consistently
remove 100% of TN, TP, or TSS, suggesting that treatment system design and proper use may
be more important factors than system type (e.g., conventional or NbS). Constructed treat-
ment wetlands achieved removal rates above the minimum threshold for all three pollutants,
while existing mangrove forests and commercial filters had lower bounds above the threshold
for TN (>40%) and TSS (>70%). The lower bound removal rates of the remaining treatment
systems were below the minimum threshold for two or more pollutants.
Comparing modelled effluent nutrient loads in this study to ASC certified farms [111] illu-
minates the potential remediation requirements necessary to achieve certification (Table 6). A
modelled nutrient waste load for L. vannamei, based on the difference between nutrients pro-
vided as feed and incorporated into shrimp biomass, found that average loading was 37.0kgN
per t and 11.7kgP per t [34]. This output suggests that average farmers would need to reduce
their nitrogen and phosphorus loads by 32% and 67%, respectively, to meet the ASC certifica-
tion standards of 25.2kgN per t and 3.9kgP per t.

Table 4. Comparisons of effluent waste loading of TN and TP across a range of stocking densities and production yields. Waste load kg shrimp-1 calculated by divid-
ing total kg ha-1 yr-1 by yield (t).
Stocking Density Yield Effluent Waste Loading TP Reference
TN
PL m-2 t ha-1 yr-1 kgN ha-1 yr-1 TN kg shirmp-1 kgP ha-1 yr-1 TP kg shrimp-1
4 1.0 128.0 128.0 40.0 40.0 [56]
4 1.0 128.0 128.0 - - [108]
6 0.2 220.7 1036.0 28.4 133.2 [109]
6 0.3 250.1 729.3 31.5 91.7 [109]
6 0.4 203.9 504.8 29.7 73.5 [109]
6 0.9 152.5 169.4 25.3 28.1 [109]
7 0.3 78.3 260.8 27.3 90.8 [26]
7 0.5 216.3 468.1 44.4 96.2 [109]
7 1.0 141.2 141.1 14.3 14.3 [109]
7 1.7 62.0 37.0* 19.0 11.7* This study
8 0.2 215.8 985.5 50.2 229.0 [109]
8 0.6 214.3 338.5 28.8 45.5 [109]
8 0.6 265.3 457.4 43.8 75.5 [109]
9 0.8 298.1 386.6 22.2 28.8 [109]
10 0.1 189.0 1592.1 27.7 233.5 [109]
10 0.5 176.2 381.4 15.6 33.8 [109]
10 0.5 193.2 411.9 14.7 31.4 [109]
10 0.6 304.0 492.8 30.8 49.9 [109]
11 0.1 187.7 1524.5 26.4 214.5 [109]
13 0.9 186.5 207.2 49.8 55.3 [26]
13 3.0 34.1 11.3 - - [108]
17 5.8 59.1 10.3 - - [108]
19 7.8 90.5 11.5 - - [108]
20 - 190.8 - 8.5 - [110]
20 - 214.3 - 7.8 - [110]
20 4.8 176.0 37.0* 56.0 11.7* This study
21 - 177.0 - 7.8 - [110]
24 6.4 73.8 11.6 - - [108]
52 13.8 199.0 14.4 39.0 2.8 [56]
52 13.8 199.0 14.4 - - [108]
58 2.0 238.5 119.3 82.5 41.3 [26]
68 21.3 934.5 44.0 302.5 14.2 [27]
71 12.1 934.5 77.4 302.5 25.1 [27]
71 17.8 934.5 52.6 302.5 17.0 [27]
71 19.4 934.5 48.3 302.5 15.6 [27]
75 21.0 777.0 37.0* 246.0 11.7* This study
120 33.6 1243.0 37.0* 393.0 11.7* This study
Notes: [108] reports dissolved inorganic nitrogen (DIN) = ([NO2 + NO3] + [NH4]), [109] includes nutrient load from water exchange and pond drainage and
calculated assuming 2.2 cycles per year, [110] calculated assuming 2.5 cycles per year, [27] includes nutrient load as total load minus shrimp harvest and calculated
assuming 2.5 cycles per year.
*TN and TP load t-shrimp-1 for this study taken from [34].

Table 5. Water quality improvements, equivalent annual costs per kg of harvested shrimp, spatial requirements, and ecosystem services associated with every treat-
ment option across each production scenario. Water quality criteria are expressed as a percentage decrease from initial condition. Equivalent annual costs assess the dis-
counted NPV over the lifespan of each treatment per kg of harvested biomass. Spatial criteria are expressed as the area in m2 necessary to treat 1 ha of production pond,
where 1 ha = 10,000m2. Select ecosystem services are presented with service value (full assessment in Table C in S1 Text). Threshold target values, shaded green, are
removal rates of at least 40%TN, 40%TP, and 70%TSS, EAC less than $0.18 kg-1, spatial requirement less than 10,000m2 (1ha), and at least ‘Medium’ ecosystem service pro-
vision. Values below targets are orange and cross-hatched cells indicate ‘not applicable’.
Treatment Treatment System Water Quality Economic Spatial Criteria Ecosystem Services
System Type (Stocking Density) Criteria Criteria
Percent decrease Equivalent Area Required Categorized as providing High, Medium, or Low service provision
from initial Annual Cost m2:1 ha of
condition USD kg-1 production
(1ha = 10,000m2)
TN TP TSS USD kg-1 m2 Cultural Regulating Provisioning Supporting Cumulative
Services Services Services Services Score
Conventional Commercial Filters NA NA NA NA NA NA NA NA
(7PL m-2 = per m2)
Commercial Filters NA NA NA
(20PL m-2 = per m2)
Commercial Filters NA NA NA
(75PL m-2 = per m2)
Commercial Filters 43– 15– 92% 0.99 30
(120 PL m-2 = per m2) 91% 84%
Woodchip Bioreactors 49– 15– 64– 0.32 10 NA NA NA NA NA
(7PL m-2 = per m2) 71% 55% 93%
Woodchip Bioreactors 0.28 20
(20PL m-2 = per m2)
(75PL m-2 = per m2)
(120 PL m-2 = per m2)
Settling Ponds 20– 22– 60– 0.26 70 L L L M L
(7PL m-2 = per m2) 31% 55% 88%
Settling Ponds 0.11 190
(20PL m-2 = per m2)
Settling Ponds 0.04 820
(75PL m-2 = per m2)
Settling Ponds 0.04 1,320
(120 PL m-2 = per m2)
(Continued )

Table 5. (Continued)
Treatment Treatment System Water Quality Economic Spatial Criteria Ecosystem Services
System Type (Stocking Density) Criteria Criteria
Percent decrease Equivalent Area Required Categorized as providing High, Medium, or Low service provision
from initial Annual Cost m2:1 ha of
condition USD kg-1 production
(1ha = 10,000m2)
TN TP TSS USD kg-1 m2 Cultural Regulating Provisioning Supporting Cumulative
Services Services Services Services Score
Nature-based Biofiltration (IMTA*) 10– 10– 10– 2.12 1,300 L L L L L
Solutions (7PL m-2 = per m2) 34% 44% 71%
Biofiltration (IMTA*) 2.02 3,540
(20PL m-2 = per m2)
(75PL m-2 = per m2)
(120 PL m-2 = per m2)
Silvoaquaculture 2– (-6)- NA 0.39 6,670 L H M M M
(7PL m-2 = per m2) 53% 46%
Silvoaquaculture NA NA NA NA
(20PL m-2 = per m2)
(75PL m-2 = per m2)
(120 PL m-2 = per m2)
Constructed 46– 60– 70– 0.25 2,710 L H M M M
(Mangrove) Wetlands 92% 100% 95%
(7PL m-2 = per m2)
Constructed 0.17 5,370
(Mangrove) Wetlands
(20PL m-2 = per m2)
(Mangrove) Wetlands
(7PL m-2 = per m2)
(Mangrove) Wetlands
(120 PL m-2 = per m2)
Existing 43– 28– 95% 0.00 630 L H M H M
Mangrove Forests 50% 48%
(7PL m-2 = per m2)
Existing 0.00 1,800
Mangrove Forests
(20PL m-2 = per m2)
Existing 0.00 7,960
Mangrove Forests
(75PL m-2 = per m2)
Existing 0.00 12,740
Mangrove Forests
(120 PL m-2 = per m2)
* IMTA generates additional revenue through secondary, or even tertiary, products which were not factored into the calculation. However, these additional
products may also incur additional capital and operating costs.
TN and TP EAC kg-1 Area < 0.6ha Medium or High Ecosystem Service Score
>40%, TSS < $0.18
>70%
TN and TP EAC kg-1 Area > 0.6ha Low Ecosystem Service Score
<40%, TSS > $0.18
<70%
NA Not NA Not NA Not NA Not Applicable
applicable applicable applicable

Table 6. Comparisons of effluent waste loading of TN and TP across a range of production yields from ASC certified farms. Annual waste load (kg ha-1 yr-1) calcu-
lated by multiplying yield (t) and nutrient load (kg t-shrimp-1). ASC certification standards require less than 25.2kgTN t-1 and less than 3.9kgP t-1. Table data from [111]
and rearranged in order of production yield.
Stocking Density Yield Effluent Waste Loading from ASC Certified Farms
TN TP
PL m-2 t ha-1 yr-1 kgN ha-1 yr-1 kgN t-shirmp-1 kgP ha-1 yr-1 kgP t-shrimp-1
- 1.6 0.0 0.0 0.0 0.0
7* 1.7 62.0 37.0 19.0 11.7
- 3.1 56.2 18.2 6.5 2.1
- 3.7 32.1 8.7 6.6 1.8
- 3.8 45.3 11.9 4.5 1.2
- 4.7 47.4 10.1 1.9 0.4
20* 4.8 176.0 37.0 56.0 11.7
- 5.2 0.5 0.1 0.3 0.1
- 16.6 306.2 18.5 42.0 2.5
- 19.0 17.1 0.9 1.3 0.1
75* 21.0 777.0 37.0 246.0 11.7
- 26.5 392.8 14.8 56.5 2.1
- 29.2 447.1 15.3 47.6 1.6
120* 33.6 1243.0 37.0 393.0 11.7
- 43.6 558.5 12.8 83.8 1.9
* Indicates modelled scenarios and outputs from this study.
Equivalent annual costs per kg

NbS treatment systems showed cost-competitiveness against conventional systems based on
EAC kg-1 values. Settling ponds, constructed wetlands, and existing mangrove forests generally
had EAC values below the USD 0.18 kg-1 threshold, while the low output of the 7 PL m-2 sce-
nario resulted in EAC values exceeding the threshold. As production yields and revenues grow
with intensification, the capital and operating costs for treatment systems decrease on a per kg
basis, indicated by falling EAC kg-1 values as stocking density increases. However, the high
capital and operating costs of the commercial filters in the 120 PL m-2 scenario exceeded the
threshold of USD 0.18 kg-1. The use of existing mangrove forests requires little capital costs
compared to other treatment systems as the mechanism for nutrient retention would already
be in place. Paired with low annual costs to monitor and maintain the forest, overall EAC val-
ues for existing mangrove forests are minimal.
Area requirements
Conventional effluent treatment systems demand a smaller spatial footprint compared to NbS
systems, which require large areas for complex biotic and abiotic processes necessary for nutri-
ent remediation. Conventional treatment systems fell well below the 0.6ha (6,000m2) thresh-
old, with most scenarios only requiring tens or hundreds of square meters per hectare of
production. NbS systems in the 7 PLm-2 and 20 PLm-2 scenarios required land area below the
0.6ha threshold but exceeded this threshold as production intensity and nutrient output
increased. IMTA biofiltration, constructed mangrove treatment wetlands, and existing man-
grove forests require 2.28ha, 1.34ha, and 1.27ha, respectively, per 1ha of production pond in
the 120 PLm-2 scenario. Silvoaquaculture exceeds the 0.6ha threshold in the 7 PLm-2 scenario

where there is a fixed ratio of 60% production pond to 40% mangrove area (i.e., 16,670m2 total
area results in 10,000m2 production area and 6,670m2 treatment area).
Ecosystem services
NbS systems, by definition, deliver more ecosystem services than conventional systems by
integrating nature and natural processes into effluent treatment. Commercial filters and wood-
chip bioreactors are not ecosystems and, thus, do not provide additional ecosystem services
but are systems that convey environmental benefits through their water quality improvements.
Meanwhile, settling ponds have been categorized as types of “human-made wetlands” that are
able to provide some ecosystem services [105]. Existing mangrove forests received the highest
cumulative score (35 out of 54) with silvoaquaculture and constructed mangrove wetlands at
31 and 30, respectively. The degree to which specific treatment systems can deliver on ecosys-
tems service sub-categories would be context dependent with larger, contiguous parcels likely
provided improved service provision over smaller, fragmented parcels.
Normalization and aggregation of performance indicators

While identifying whether specific performance criteria are above or below a given threshold
is useful when trying to evaluate specific attributes, it does little to provide a comparison of
treatment systems as a whole. Normalizing values across a vector between 0 and 1.00 within
each performance indicator allows for relative comparisons when units vary across perfor-
mance indicators. An aggregated indicator value, using the normalized criterion value and
equal weighting for all indicators, provides a single output that is used to rank the conventional
and NbS treatment systems for production intensities of 7 PLm-2 (Table 7), 20 PLm-2
(Table 8), 75 PLm-2 (Table 9), and 120 PLm-2 (Table 10). Although values within specific
Table 7. Normalization and aggregation of treatment system indicators at a stocking density of 7 PL m-2.
Treatment Systems Treatment System Type Mean Value TN TP TSS EAC m2 Ecosystem Services
Existing Mangrove Forests NbS 0.73 0.45 0.29 1.00 1.00 0.97 0.66
Constructed (Mangrove) Wetlands NbS 0.71 0.48 0.63 0.74 0.89 0.88 0.66
Threshold 0.65 0.42 0.42 0.74 0.92 0.74 0.66
Settling Ponds Conventional 0.55 0.21 0.23 0.63 0.88 1.00 0.33
Woodchip Bioreactors Conventional 0.53 0.52 0.16 0.67 0.85 1.00 0.00
Silvoaquaculture NbS 0.37 0.02 0.00 0.00 0.82 0.71 0.66
Biofiltration (IMTA) NbS 0.27 0.11 0.11 0.11 0.03 0.94 0.33
Commercial Filters Conventional NA NA NA NA NA NA NA
Threshold 0.65 0.42 0.42 0.74 0.92 0.74 0.66
Silvoaquaculture NbS NA NA NA NA NA NA NA

Threshold 0.65 0.42 0.42 0.74 0.92 0.74 0.66
Threshold 0.65 0.42 0.42 0.74 0.92 0.74 0.66
Commercial Filters Conventional 0.52 0.45 0.16 0.97 0.55 1.00 0.00
indicators may be above or below a given threshold, existing mangrove forests and constructed
mangrove wetlands consistently ranked as the treatment systems with the top overall aggre-
gated values. In all cases, except the 120 PLm-2 scenario, these types of treatment systems were
ranked above the threshold value.
The ranking yields a single system with the highest aggregate value, however, the purpose of
this study is to illicit a short-listed set of options that practitioners can use for further investiga-
tion [112]. Caution should be taken when comparing removal rates, economic factors, spatial
requirements, and ecosystem service provision of different treatments due to the model’s
dependence on specific conditions and environmental characteristics drawn from literature,
which will differ depending upon the characteristics of the site, species of study, and cultiva-
tion practices being employed within and across production systems.
Discussion
This analysis provides theoretical economic and environmental assessments of shrimp farm
effluent treatment systems to compare their costs and benefits across a range of production
scenarios. The conceptual approach of modelling these scenarios is intended to provide the
foundation for further evaluation and would benefit from in situ farm data to better compare
conventional and NbS treatment systems at commercial production levels.
Estimated nutrient loading

Nutrient effluents in shrimp aquaculture are commonly reported as a mass load or concentra-
tion, but either alone has limitations for assessing potential environmental impacts [36]. For
example, mass loading (e.g., kg of nutrient ha-1 or t-1) does not capture discrete time periods,

such as pulses of effluent associated with complete pond drainage while harvesting shrimp.
Conversely, while concentrations (e.g., mg/L or ppm) are important to understand nutrient
solutes at a given point in time, they are less accurate in assessing total nutrients leaving the
production system if samples are used to estimate average concentrations over the production
cycle. Nutrient concentrations are also a function of farm-level water management, such that
increased flushing or more frequent water exchange can decrease nutrient concentrations in
effluent but could still be accounted for in total mass. In practice, water quality management
should be informed by nutrient loads, nutrient concentrations, and water use throughout the
production cycle and harvest for a comprehensive understanding of localized effluent
management.
Reported nutrient loading for shrimp aquaculture in the literature tended to be from older
studies and lower stocking densities. While our TN (62 kgN ha-1 yr-1) and TP (19 kgP ha-1
yr-1) loading for the 7PLm-2 scenario was plausible given the range of previously reported val-
ues at the same stocking density (78–216 kgN ha-1 yr-1 and 14–44 kgP ha-1 yr-1) [26,109], both
were towards the lower bounds. TN loading at the 20 PLm-2 scenario was also at the lower end
of reported values (177–214 kgN ha-1 yr-1) [110], but the modelled TP loading of 56 kgP ha-1
yr-1 was much higher than the 7.8–8.5 kgP ha-1 yr-1 found in a previous study [110]. However,
TP loading of 50 kgP ha-1 yr-1 was reported for a stocking density of 13 PLm-2 [26], indicating
a wide possible range under different production conditions. A stocking density of 71 PLm-2
with effluent loading of 935 kgN ha-1 yr-1 and 303 kgP ha-1 yr-1 [27] was the closest to compare
to the 75 PLm-2 scenario, which was found to be slightly lower at 777 kgN ha-1 yr-1 and
246 kgP ha-1 yr-1, respectively. Effluent loading approaching 120 PLm-2 was not found in pub-
lished literature. While audit data from ASC certified farms are available and have been pub-
lished [111], the reported values have already undergone some level of effluent treatment, and
thus, wouldn’t be appropriate for input values for the evaluated treatment systems.
Previous studies have utilized a nutrient mass balance approach to estimate total effluent
loading [23,24,26,28,110], accounting for all nutrient inputs (e.g., feed, influent water, fertiliz-
ers, earthen ponds, stocked shrimp, etc.) and nutrient outputs (e.g., effluent water, seepage,
denitrification, sediments, harvested shrimp, etc.). This approach is useful to gather empirical
farm data but is limited in use to model scenarios given the change in input variables, pond
chemistry, and resulting output values under a range of production intensities. Another
approach, as used in this study, is to estimate nutrient waste loading using FCR and the differ-
ence between the decimal fraction of nitrogen or phosphorus in feed minus the decimal frac-
tion of nitrogen or phosphorus in the live weight of the cultured animals [34]. This assumes
that feed is the major nutrient input and that the nitrogen and phosphorus not utilized in
shrimp biomass is discharged into the environment. Outputs from nutrient effluent modelling,
regardless of the methodology, would be better supported with farm-level data and should be
used cautiously given the diversity of geographies and production systems that shrimp aqua-
culture occupies.
Estimating a generic, or “average” nutrient composition of effluent is further complicated
by a range of farm-level practices during the production cycle that can directly impact nutrient
concentration, nutrient loading, and water use. Feed formulations and ingredient composition
affect water quality [113], while macroaggregate formations of microorganisms (biofloc)
enhance water quality by uptake of nitrogen compounds generated by microbial growth and
competing for resources with pathogens [114]. Additives, like probiotics, protect shrimp from
opportunistic pathogens [115] while having bioremediation benefits. These types of manage-
ment approaches to maintain pond water quality during the production cycle vary widely
from one farmer to another and, thus, were not included in the study. Settling ponds are com-
monly employed for effluent remediation, and have been found to be effective in reducing

TSS, but are less effective for reducing TN due to dissolved nitrogen compounds that do not
settle–indicating that a more holistic approach to water quality management is necessary to
mitigate nutrient discharge [25].
Water quality criteria

Identifying a universal metric for ‘effective’ nutrient removal is challenging and the reported
removal rates assembled from literature are highly context dependent. While none of the eval-
uated treatment systems were found to remove 100% of nutrient pollutants, the degree to
which effluent impacts waterways depends on the assimilative capacity of the receiving water
to absorb excess nutrients, which can be a function of temperature, current speed, biotic fac-
tors, and other sources of nutrient inputs [33]. Further, the ‘effective’ amount of nutrient
release into a water body for one farm is a function of the nutrient releases of all farms and
other sources on that water body. Jurisdictional-level regulations and initiatives are critical for
responsible intensification beyond the individual farm-level, given the high degree of surface
water connectivity between most farms, which can affect water quality and disease prevalence
[116,117]. Sustainable aquaculture practices must adopt effective and affordable wastewater
treatment processes to address the full range of environmental risks as the sector grows and
intensifies [118], taking into account physical, production, ecosystem, and social carrying
capacities [119].
Removal rates collected through literature review for the evaluated treatment systems indi-
cate that a 32% reduction in TN for the 120PLm-2 scenario to achieve ASC certification stan-
dards may be achievable for most treatment systems, but that a 67% reduction in TP is outside
of the upper threshold reported in many studies. However, simply applying removal rates
found in literature oversimplifies the comprehensive farm management practices necessary to
reduce effluent loads. Farms would need to implement numerous water quality monitoring
and management protocols to make meaningful improvements, and it may be that larger,
more corporate farms are better equipped to achieve these targets and comply with interna-
tional certification standards [111].
Equivalent annual costs per kg and financial considerations

Farm financial performance is highly variable based on production and market parameters,
and assumptions used to generate revenue in this study should be adjusted for specific geogra-
phies and farm performance. For example, crop duration and number of production cycles
per year vary across production systems and are dependent on management practices as well
as disease prevalence. The impact of mortality on revenue and profit is a function of timing,
and the assumption that mortality occurs at the beginning of the production cycle may slightly
overestimate revenue, while the impact on profitability could be more significant.
Substantial profit margins are necessary for farmers to implement effluent treatments sys-
tems, which were found to be more difficult to obtain for low-intensity producers. Many of the
treatment system EACs for the 7PLm-2 scenario were above the cost threshold, while increas-
ing production intensity resulted in lower relative costs on a per kg shrimp basis. Profit mar-
gins fluctuate based on internal and external factors, such as farm efficiency, input costs, and
market prices. Average profits have been found to range from about 16% EBIT in Indonesia to
about 20% EBIT in Thailand, Vietnam, and India for L. vannamei [13,120–122]. The selected
threshold of USD 0.18 kg shrimp-1, or about 4% of EBIT, may be a significant diversion of rev-
enue for average farmers to invest in effluent treatment, however, farm-level improvements,
such as improved growth through better feed and the use of biofloc, can increase EBIT mar-
gins from 16% up to 23% and 21%, respectively, in Indonesia [13]. This suggests that the

increased profit from improved farm management could cover the capital and operating costs
necessary to remediate effluent outflow.
EAC calculations for constructed mangrove wetlands could be highly variable depending
on localized restoration costs, which would require restoring production ponds or degraded
areas back into mangrove habitat, incurring costs for design, labor, materials, and time.
Depending on location, economic situation of the project host country, and initial condition
of the restoration site, these costs can range from as high as USD 125,000 per ha in developed
countries or as low as USD 100–1000 per ha in developing countries [123,124]. The effective
removal rates and low operating costs of constructed mangrove wetlands make them viable
solutions for developing countries in tropical climates [125], but project-specific costs need to
be considered.
Several treatment systems presented in this study provide supplemental revenue sources
that could offset some of the treatment costs. IMTA typically combines high-value target spe-
cies (i.e., shrimp) with secondary extractive species, such as shellfish or seaweeds, which can be
sold as feed, fertilizers, or for human consumption. Supplemental revenue would be especially
important for IMTA since our results indicated that it is the treatment system with much
higher overall costs. Additional fish and crustacean species can enter silvoaquaculture produc-
tion areas providing up to 24% in additional yields and 14% in supplemental income [126].
Intact and restored mangrove forests could benefit from emerging blue carbon finance mecha-
nisms, such as voluntary carbon credits. However, only a few mangrove conservation and res-
toration projects, including one recently led by Conservation International in the Bay of
Cispatá, Colombia [127], have issued Verified Blue Carbon Units. Due to the variability across
and within these systems to generate supplemental revenue, these benefits were not quantified
in the study but could provide additional incentives.
Spatial requirements
The spatial requirements for NbS treatment options vary greatly, reflecting the variation of their
removal efficiencies across, as well as within, systems [125]. Our results of 1.3ha of mangroves
are slightly lower than previous studies that have suggested an area between 1.8ha and 21.7ha of
existing mangrove forests needed for every one hectare of production pond [56,69,128]. The
spatial requirements for existing mangroves are limited by their environmental capacity to miti-
gate effluent nutrients when considering clustered farm densities and local regulations on man-
grove use [129]. The shared use of limited off-farm mangrove forests could create a scenario of
over-pollution and over-saturation of nutrients without adequate and enforceable regulatory
intervention. Spatial requirements for constructed mangrove wetlands used for wastewater
treatment vary considerably as well. An area of just 0.086ha has been recommended for a stock-
ing density of 100 PLm-2 [130] but ranges up to 12ha for intensive shrimp production [57],
aligning with the 1.34ha findings for the 120 PLm-2 scenario of this study.
Opportunity costs of land dedicated to effluent treatment rather than production area rep-
resents a significant financial consideration for farmers. Land suitable for shrimp ponds, typi-
cally above tidal influence, are the most valuable to a farmer. Surplus land on a farm tends to
be intertidal or otherwise unsuitable for production, and it is in these areas that NbS treatment
options are most viable as low-cost, easy to implement risk buffers. However, the area of sur-
plus land is often limited and not likely adequate to remediate effluent loads. Low-productivity
ponds, or those that have been abandoned, can be viable options to implement NbS. Produc-
tivity tends to decrease over time for farms that are not properly managed, with typical life-
spans of 10 to 13 years, but can be as low as one year, and after which they are likely to be
abandoned [131]. Available parcels to implement NbS at scale remains a challenge, though

sustainable intensification on a portion of a farm could sustain economic viability for farmers
while creating sufficient area for NbS systems on the remaining portion of the farm [132].
Ecosystem services and benefits to the environment

Ecosystem services provide environmental benefits to individuals and communities but are
often difficult to quantify financially as excludable goods. Attempts to standardize ecosystem
service valuation often results in wide ranges of values across and within biomes [133], due to
differing stakeholder perceptions and willingness to pay for such services [134]. Classifying
ecosystem service benefits by beneficiary (i.e., individual, group, community, etc.) addresses
some heterogeneity [135], but the monetary value that an individual farm may gain from eco-
system services is challenging to determine, making it an unconvincing value proposition for
farmers to invest in. Additional financial structures and mechanisms are needed that can cap-
ture the value of ecosystem services, for the individual and community, to incentivize farmers
towards supporting such initiatives.
Conventional, or gray, infrastructure, while effective for their designed purpose, does not
provide additional ecosystem services and can have negative environmental impacts as a result
of degraded surrounding natural ecosystems, resource and energy use, or other waste outputs
[7]. Both commercial filters and woodchip bioreactors were found to have a small footprint to
be effective at any given production intensity, relative to other treatment systems. However,
commercial filters have high energy requirements to pump water and have resource-intensive
parts with finite lifespans that will need to be replaced. Woodchip bioreactors require a com-
plete replacement of woodchip media at least once every 5 years [55]. Although settling ponds
can include building materials when lined with plastic or cement, many are earthen basins that
can be defined as human-made wetlands with the potential for minimal ecosystem service pro-
vision [105].
Approximately 52% of mangroves across Asia and South America have been deforested
since 1970, with shrimp aquaculture expansion accounting for 28% of that loss [19, 136], and
up to 63% to 76% of loss at a provincial level [19,20]. Although the rates of mangrove defores-
tation have decreased from as high as 3.6% per year to 0.05–0.7% per year over the last two
decades [19,137,138], the multitude of benefits provided by intact mangrove forests remain
absent. Silvoaquaculture may achieve additional mangrove area, but the widespread imple-
mentation in areas such as the Mekong Delta has led to increased mangrove forest fragmenta-
tion [139] with limited benefits to overall ecosystem services. Over-reliance on the natural
remediation capacity of existing mangroves forests comes with significant risks, potentially
having adverse effects for the ecosystems services they provide. Recent attention has been
directed towards the impacts of effluent on soil composition and carbon stocks, where contin-
ual aquaculture effluent has driven cumulative increases in soil nutrients, increased emissions,
and contributed to localized eutrophication potential [140–144]. Cumulative impacts, includ-
ing effects to aquatic food webs, from high-production areas as seen in Asia, likely have signifi-
cantly larger influence on natural nitrogen cycling than previously anticipated [35]. The use of
existing mangrove forests to abate large volumes of unregulated aquaculture effluent has limi-
tations and the adverse impacts to ecosystem service delivery warrants additional attention.
However, many of these complications can be addressed if mangrove ecosystems can be
appropriately designed to mitigate effluents using constructed treatment wetlands. For exam-
ple, treatment wetlands have been proposed to be built within existing ponds when space is
limited by compacting the bottom and creating new berms, therein providing deep basins to
extend hydraulic residence time and increase contact surface area between the effluent, soil
matrix, and root zone [130].

Widespread adoption of NbS in the aquaculture sector depends upon building the evidence
that validates such an approach and growing the experience of engineers, contractors, and gov-
ernments to finance and implement NbS projects. While concepts that integrate NbS, such as
hybrid green-gray infrastructure, are emerging they are not yet in common use [145]. How-
ever, early examples show promise, such as converting cultivated land back into mangrove
ecosystems to help manage coastal retreat and erosion [146] as well as shrimp farming that
supports Climate Compatible Development [147] where “mixed production systems” of aqua-
culture and mangrove restoration take place simultaneously [148]. One obstacle to wide-
spread adoption is the lack of information that decision makers have to robustly and efficiently
compare the performance of conventional and NbS alternatives to make informed investment
choices. Transparent and honest communication within and across sectors on the efficacy of
NbS pilots, innovations, and applications should be encouraged to help facilitate the use of
conventional and NbS approaches where appropriate.
Areas for further research

In general, there is a lack of robust data on shrimp farm effluent loads and treatment systems.
Effluent waste loads in this analysis were calculated based on production assumptions that will
vary across producers, geographies, and time. Findings from this study allude to the potential
costs and benefits of conventional and NbS treatment systems but would benefit from further
validation through actual farm-level effluent data and side-by-side treatment comparisons.
Specifically for constructed mangrove wetlands, where characteristics of the wetland changes
as mangroves mature, additional data is needed to understand the remediation potential and
ecosystem service provision over the lifetime of the system.
Existing analyses evaluating commercial applications of NbS for effluent treatment and
environmental benefits are sparse, however, initial results are encouraging. A 10-year pilot
constructed wetland system in the Pearl River Delta of China designed to treat municipal
wastewater recently observed that two mangrove species maintained a steady and efficient
treatment performance and did not require additional harvesting, replanting, or maintenance,
whereas herbaceous vascular plants may incur addition maintenance costs and variable
removal efficiencies [91,149]. In another case, 120ha of mangrove wetland used to treat efflu-
ent from 286ha of shrimp farms in Colombia found that the system was effective in eliminating
suspended solids and that a large and resident bird population had developed [150]. Continu-
ous aquaculture effluent has been found to cause elevated soil organic carbon, TN, and TP in
proximity to discharge point sources, but these concentrations rapidly decreased through
300m of mangrove stands [140]. However, the study warned that carbon sequestration poten-
tial could be impacted from long-term nutrient inputs if mangrove forests were too small to
fully treat effluent. Conversely, accumulation of TN and TP by Sonneratia apetala Buch-Ham
indicated an increase of 50% in biomass with higher wastewater concentration and demon-
strated a linear correlation between mangrove biomass and nutrient inputs [151]. Additional,
long-term research on the bioremediation capacity of mangroves to mitigate nutrient effluent
from commercial aquaculture is needed to document the potential benefits and trade-offs
associated with constructed mangrove treatment wetlands.
Future studies of aquaculture effluent management should consider different combinations
of hybrid treatments for commercial application. While modelled effluent treatments showed
promise individually, our approach does not allow for the use of hybridizing treatments in
sequence or in parallel due to the increasing complexity of biogeochemical processes interact-
ing with the effluent from one treatment to the next. Although we would anticipate that hybrid
treatment methods, like using settling ponds before constructed mangrove wetlands, would

confer ways of balancing tradeoffs and constraints of either treatment individually, a lack of
water quality data inhibits the assessment of such an approach.
Conclusions
As shrimp aquaculture production intensifies, treatment of effluent is critical to minimize and
avoid negative impacts to surrounding aquatic environments. Constructed mangrove wetlands
are an NbS approach that can meet the intensification needs of aquaculture producers and
reduce negative impacts from effluent at competitive costs, while also providing ecosystem ser-
vice co-benefits. However, limited availability of parcels to implement NbS remain a major
obstacle and alternative incentives for farms, such as sustainably intensifying in a smaller farm-
ing footprint and restoring mangroves on unused parcels, will need to be explored for shrimp
farmers to realize potential benefits and utilize such systems. Additional studies and pilots are
needed to inform practitioners and policymakers on the diversity of NbS applications and to
gain larger stakeholder acceptance and support.
Supporting information
S1 Text. Supplementary methods.
(DOCX)
Acknowledgments
The authors would like to acknowledge the technical assistance and input provided by Jan
Yoshioka, Gracie White, Ana Plana Casado, Jonah Busch, Starry Sprenkle-Hyppolite, Rod
Braun, Joe Schmidt, Kate Hewitt, and Pat Megonigal. Fig 1 drawing by Amy West.
Author Contributions
Conceptualization: Garrett M. Goto, Emily Corwin, Dane H. Klinger.
Data curation: Garrett M. Goto, Emily Corwin, Alexander Farthing, Anisa Rilla Lubis, Dane
H. Klinger.
Investigation: Garrett M. Goto, Emily Corwin, Alexander Farthing, Anisa Rilla Lubis, Dane
H. Klinger.
Methodology: Garrett M. Goto.
Writing – original draft: Garrett M. Goto.
Writing – review & editing: Garrett M. Goto, Emily Corwin, Alexander Farthing, Anisa Rilla
Lubis, Dane H. Klinger.
References
1. FAO. Fishery and Aquaculture Statistics. Global aquaculture production 1950–2020 (FishStatJ) [Inter-
net]. FAO Fisheries and Aquaculture Division (online); 2022. www.fao.org.fishery/statistics/software/
fishstat/en
2. IUCN. WCC-2016-Res-069 [Internet]. World Conservation Congress; 2016. https://portals.iucn.org/
library/sites/library/files/resrecfiles/WCC_2016_RES_069_EN.pdf
3. UNEP. UNEP and Nature-based Solutions [Internet]. 2020. https://www.unep.org/unep-and-nature-
based-solutions
4. Hughes AD. Defining Nature-Based Solutions Within the Blue Economy: The Example of Aquaculture.
Front Mar Sci [Internet]. 2021 Jul 29 [cited 2021 Oct 22]; 8:711443. Available from: https://www.
frontiersin.org/articles/10.3389/fmars.2021.711443/full

5. Le Gouvello R, Brugère C, Simard F. Aquaculture and Nature-based Solutions: identifying synergies

between sustainable development of coastal communities, aquaculture, and marine and coastal con-
servation [Internet]. IUCN, International Union for Conservation of Nature; 2022 Feb [cited 2023 Jan
11]. https://portals.iucn.org/library/node/49887
6. Browder G, Ozment S, Bescos IR, Gartner T, Lange GM. Integrating Green and Gray: Creating Next
Generation Infrastructure [Internet]. Washington, D.C.: World Bank and World Resources Institute;
2019 Mar p. 140. https://www.wri.org/publication/integrating-green-gray
7. Thiele T, Alleng G, Biermann A, Corwin E, Crooks S, Fieldhouse P, et al. Blue Infrastrucutre Finance:
A new aproach, integrating NAture-based Solutions for coastal resilience. Gland, Switzerland: IUCN;
2020 Mar.
8. OECD. Climate-resilient Infrastructure. OECD; 2018 Dec. Report No.: No. 14.
9. Lekang OI. Aquaculture Engineering, 2nd Edition. 2nd ed. Norway: Wiley-Blackwell; 2013.
432 p.
10. Halim D, Juanri. Indonesia’s Aquaculture Industry. Key Sectors for Future Growth [Internet]. France:
IPSOS Business Consulting; 2016 Aug p. 1–11. Report No.: V11 08232016. https://www.ipsos.com/
sites/default/files/2016-08/indonesia-aquaculture-industry.pdf
11. Engle CR, McNevin A, Racine P, Boyd CE, Paungkaew D, Viriyatum R, et al. Economics of Sustain-
able Intensification of Aquaculture: Evidence from Shrimp Farms in Vietnam and Thailand. J World
Aquac Soc [Internet]. 2017 Apr 1 [cited 2020 Nov 12]; 48(2):227–39. Available from: https://doi.org/10.
1111/jwas.12423
12. CEA. Shrimp Aquaculture Landscape. California Environmental Associates; 2018 Jan.
13. Rubel H, Woods W, Pérez D, Unnikrishnan S, Meyer Zum Felde A, Zielcke S, et al. A Strategic
Approach to Sustainable Shrimp Production in Indonesia: The Case for Improved Economics and Sus-
tainability. Boston Consulting Group; 2019 Nov. Report No.: Indonesia.
14. Davis R, Abebe A, Boyd C, McNevin A. Exploring the relationship between production intensity and
land use: A meta-analytic approach with shrimp aquaculture. J Environ Manage [Internet]. 2021 Dec
[cited 2022 Jan 5]; 300:113719. Available from: https://linkinghub.elsevier.com/retrieve/pii/
S0301479721017813 https://doi.org/10.1016/j.jenvman.2021.113719 PMID: 34521002
15. Joffre OM, Poortvliet PM, Klerkx L. Are shrimp farmers actual gamblers? An analysis of risk perception
and risk management behaviors among shrimp farmers in the Mekong Delta. Aquaculture [Internet].
2018 Oct [cited 2021 Nov 1]; 495:528–37. Available from: https://linkinghub.elsevier.com/retrieve/pii/
S0044848618301108
16. Henriksson PJG, Belton B, Jahan KM e, Rico A. Measuring the potential for sustainable intensification
of aquaculture in Bangladesh using life cycle assessment. Proc Natl Acad Sci [Internet]. 2018 Mar 20;
115(12):2958. Available from: http://www.pnas.org/content/115/12/2958.abstract
17. Davis RP, Boyd CE, Davis DA. Resource sharing and resource sparing, understanding the role of pro-
duction intensity and farm practices in resource use in shrimp aquaculture. Ocean Coast Manag.
2021;(207):7.
18. Naylor RL, Goldberg R, Primavera J, Kautsky N, Beveridge M, Clay J, et al. Effect of aquaculture on
world fish supplies. Nature. 2000 Jun 29; 405:1017–24. https://doi.org/10.1038/35016500 PMID:
10890435
19. Friess DA, Rogers K, Lovelock CE, Krauss KW, Hamilton SE, Lee SY, et al. The State of the World’s
Mangrove Forests: Past, Present, and Future. Annu Rev Environ Resour [Internet]. 2019 Oct 17 [cited
2020 Oct 23]; 44(1):89–115. Available from: https://www.annualreviews.org/doi/10.1146/annurev-
environ-101718-033302
20. Herbeck LS, Krumme U, Andersen TJ, Jennerjahn TC. Decadal trends in mangrove and pond aqua-
culture cover on Hainan (China) since 1966: mangrove loss, fragmentation and associated biogeo-
chemical changes. Estuar Coast Shelf Sci [Internet]. 2020 Feb [cited 2020 Oct 23]; 233:106531.
Available from: https://linkinghub.elsevier.com/retrieve/pii/S027277141830372X
21. Naylor RL, Hardy RW, Buschmann AH, Bush SR, Cao L, Klinger DH, et al. A 20-year retrospective
review of global aquaculture. Nature [Internet]. 2021 Mar 25 [cited 2021 Apr 15]; 591(7851):551–63.
Available from: http://www.nature.com/articles/s41586-021-03308-6 https://doi.org/10.1038/s41586-
021-03308-6 PMID: 33762770
22. Ottinger M, Clauss K, Kuenzer C. Aquaculture: Relevance, distribution, impacts and spatial assess-
ments—A review. Ocean Coast Manag [Internet]. 2016 Jan [cited 2020 Jun 11]; 119:244–66. Available
from: https://linkinghub.elsevier.com/retrieve/pii/S0964569115300508
23. Briggs MRP, Funge-Smith SJ. A nutrient budget of some intensive marine shrimp ponds in Thailand.
Aquac Res [Internet]. 1994 Oct [cited 2020 Jun 15]; 25(8):789–811. Available from: http://doi.wiley.
com/10.1111/j.1365-2109.1994.tb00744.x

24. Funge-Smith SJ, Briggs MRP. Nutrient budgets in intensive shrimp ponds: implications for sustainabil-
ity. Aquaculture [Internet]. 1998 May [cited 2020 May 18]; 164(1–4):117–33. Available from: https://
linkinghub.elsevier.com/retrieve/pii/S0044848698001811
25. Jackson CJ, Preston N, Burford MA, Thompson PJ. Managing the development of sustainable shrimp
farming in Australia: the role of sedimentation ponds in treatment of farm discharge water. Aquaculture
[Internet]. 2003 Oct [cited 2020 May 4]; 226(1–4):23–34. Available from: https://linkinghub.elsevier.
com/retrieve/pii/S0044848603004642
26. Páez-Osuna F, Ruiz-Fernández AC. Environmental Load of Nitrogen and Phosphorus from Extensive,
Semiintensive, and Intensive Shrimp Farms in the Gulf of California Ecoregion. Bull Environ Contam
Toxicol [Internet]. 2005 Apr [cited 2020 Jul 1]; 74(4):681–8. Available from: http://link.springer.com/10.
1007/s00128-005-0637-8 https://doi.org/10.1007/s00128-005-0637-8 PMID: 16094882
27. Huy Van Nguyen Morihiro Maeda. Nutrient Mass Balances in Intensive Shrimp Ponds with a Sludge
Removal Regime: A Case Study in the Tam Giang Lagoon, Central Vietnam. J Agric Sci Technol A
[Internet]. 2015 Dec 28 [cited 2020 May 18]; 5(12). Available from: http://www.davidpublisher.org/
index.php/Home/Article/index?id=25949.html
28. Chaikaew P, Rugkarn N, Pongpipatwattana V, Kanokkantapong V. Enhancing ecological-economic
efficiency of intensive shrimp farm through in-out nutrient budget and feed conversion ratio. Sustain
Environ Res [Internet]. 2019 Dec [cited 2020 Jun 10]; 29(1):28. Available from: https://
sustainenvironres.biomedcentral.com/articles/10.1186/s42834-019-0029-0
29. Prawitwilaikul O, Limsuwan C, Taparhudee W, Chuchird N. A Comparison of Rearing Pacific White
Shrimp (Liptopenaeus vannamei Boone, 1931) in Earthen Ponds and in Ponds Lined with Polyethyl-
ene. Kasetsart J Nat Sci. 2006; 40:167–71.
30. Serrano-Grijalva L, Sánchez-Carrillo S, Angeler DG, Sánchez-Andrés R, Álvarez-Cobelas M. Effects
of shrimp-farm effluents on the food web structure in subtropical coastal lagoons. J Exp Mar Biol Ecol
[Internet]. 2011 Jun 15; 402(1):65–74. Available from: https://www.sciencedirect.com/science/article/
pii/S0022098111001316
31. Bui TD, Luong-Van J, Austin CM. Impact of Shrimp Farm Effluent on Water Quality in Coastal
Areas of the World Heritage-Listed Ha Long Bay. Am J Environ Sci [Internet]. 2012 Oct 1 [cited
2020 Oct 21]; 8(2):104–16. Available from: http://www.thescipub.com/abstract/10.3844/ajessp.
2012.104.116
32. Barraza-Guardado RH, Arreola-Lizárraga JA, López-Torres MA, Casillas-Hernández R, Miranda-
Baeza A, Magallón-Barrajas F, et al. Effluents of Shrimp Farms and Its Influence on the Coastal Eco-
systems of Bahı́a de Kino, Mexico. Sci World J [Internet]. 2013 [cited 2020 Oct 21];2013:1–8. Available
from: http://www.hindawi.com/journals/tswj/2013/306370/
33. Herbeck LS, Unger D, Wu Y, Jennerjahn TC. Effluent, nutrient and organic matter export from shrimp
and fish ponds causing eutrophication in coastal and back-reef waters of NE Hainan, tropical China.
Cont Shelf Res [Internet]. 2013 Apr [cited 2020 Jun 11]; 57:92–104. Available from: https://linkinghub.
elsevier.com/retrieve/pii/S0278434312001288
34. Chatvijitkul S, Boyd CE, Davis DA, McNevin AA. Pollution potential indicators for feed-based fish and
shrimp culture. Aquaculture [Internet]. 2017 Aug [cited 2020 Nov 12]; 477:43–9. Available from:
https://linkinghub.elsevier.com/retrieve/pii/S0044848617308244
35. Herbeck LS, Krumme U, Nordhaus I, Jennerjahn TC. Pond aquaculture effluents feed an anthropo-
genic nitrogen loop in a SE Asian estuary. Sci Total Environ [Internet]. 2021 Nov [cited 2020 Dec
4];144083. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0048969720376142
36. Yeo SE, Binkowski FP, Morris JE. Aquaculture Effluents and Waste By-Products: Characterisitcs,
Potential Recovery, and Beneficial Reuse. Wisconsin Sea Grant; 2004 Aug p. 61.
37. Thompson E, Herbeck LS, Jennerjahn TC. The end of resilience: Surpassed nitrogen thresholds in
coastal waters led to severe seagrass loss after decades of exposure to aquaculture effluents. Mar
Environ Res. 2020; 160.
38. David CPC, Sta. Maria YY, Siringan FP, Reotita JM, Zamora PB, Villanoy CL, et al. Coastal pollution
due to increasing nutrient flux in aquaculture sites. Environ Geol [Internet]. 2009 Jul [cited 2021 Apr 7];
58(2):447–54. Available from: http://link.springer.com/10.1007/s00254-008-1516-5
39. Bao W, Zhu S, Jin G, Ye Z. Generation, characterization, perniciousness, removal and reutilization of
solids in aquaculture water: a review from the whole process perspective. Rev Aquac [Internet]. 2019
Nov [cited 2020 Jun 11]; 11(4):1342–66. Available from: https://onlinelibrary.wiley.com/doi/abs/10.
1111/raq.12296
40. White P. Aquaculture Pollution: An Overview of Issues with a Focus on China, Vietnam, and the Philip-
pines. Washington, D.C: Prepared for the World Bank; 2017.
41. Boyd CE, D’Abramo LR, Glencross BD, Huyben DC, Juarez LM, Lockwood GS, et al. Achieving sus-
tainable aquaculture: Historical and current perspectives and future needs and challenges. J World

Aquac Soc [Internet]. 2020 Jun 1 [cited 2020 Nov 12]; 51(3):578–633. Available from: https://doi.org/
10.1111/jwas.12714
42. Troell M, Naylor RL, Metian M, Beveridge M, Tyedmers PH, Folke C, et al. Does aquaculture add resil-
ience to the global food system? Proc Natl Acad Sci [Internet]. 2014 Sep 16; 111(37):13257. Available
from: http://www.pnas.org/content/111/37/13257.abstract https://doi.org/10.1073/pnas.1404067111
PMID: 25136111
43. Kumar G, Engle CR. Technological Advances that Led to Growth of Shrimp, Salmon, and Tilapia
Farming. Rev Fish Sci Aquac [Internet]. 2016 Apr 2; 24(2):136–52. Available from: https://doi.org/10.
1080/23308249.2015.1112357
44. FAO. Fishery and Aquaculture Statistics. Global production source 1950–2021 (FishStatJ) [Internet].
In: FAO Fisheries and Aquaculture Department (Online); 2023. www.fao.org/fishery/statistics/
software/fishstatj/en
45. Surtida A. A glimpse at shrimp culture in Indonesia. SEAFDEC Asian Aquac. 2000 Dec; XXII(6):24–5.
46. BAPPENAS. Development of Leading Strategic Commodities of Culture Fishery and Licensing Gover-
nance to Investment. Sustainable Aquaculture Fisheries Development Workshop; 2019 Sep; Jakarta,
Indonesia.
47. Asche F, Anderson JL, Botta R, Kumar G, Abrahamsen EB, Nguyen LT, et al. The economics of
shrimp disease. J Invertebr Pathol [Internet]. 2020 May 21;107397. Available from: http://www.
sciencedirect.com/science/article/pii/S0022201120301038 https://doi.org/10.1016/j.jip.2020.107397
PMID: 32446865
48. Engle CR, Quagrainie KK, Dey MM. The international market for seafood and aquaculture products.
In: Seafood and Aquaculture Marketing Handbook. John Wiley & Sons, Ltd; 2017.
49. Boyd CE, Davis RP, McNevin AA. Perspectives on the mangrove conundrum, land use, and benefits
of yield intensification in farmed shrimp production: A review. J World Aquac Soc [Internet]. 2021 Aug
11 [cited 2022 Jan 5];jwas.12841. Available from: https://onlinelibrary.wiley.com/doi/10.1111/jwas.
12841
50. McNevin A, Viskin T, Ciccaglione K, Resing N. Future Proofing Shrimp Production. Transition to Con-
trolled Intensification. Washington, D.C.: World Wildlife Fund; 2020.
51. Iber BT, Kasan NA. Recent advances in Shrimp aquaculture wastewater management. Heliyon
[Internet]. 2021 Nov [cited 2023 Jan 11]; 7(11):e08283. Available from: https://linkinghub.elsevier.
com/retrieve/pii/S2405844021023860 https://doi.org/10.1016/j.heliyon.2021.e08283 PMID:
34778576
52. Teichert-Coddington DR, Rouse DB, Potts A, Boyd CE. Treatment of harvest discharge from intensive
shrimp ponds by settling. Aquac Eng [Internet]. 1999 Feb [cited 2020 Oct 27]; 19(3):147–61. Available
53. Eding EH, Kamstra A, Verreth JAJ, Huisman EA, Klapwijk A. Design and operation of nitrifying trickling
filters in recirculating aquaculture: A review. Aquac Eng [Internet]. 2006 May [cited 2021 Apr 8]; 34
(3):234–60. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0144860905001305
54. Ngo HH, Guo W, Tram Vo TP, Nghiem LD, Hai FI. Aerobic Treatment of Effluents From the Aquacul-
ture Industry. In: Current Developments in Biotechnology and Bioengineering: Biological Treatment of
Industrial Effluents [Internet]. Elsevier; 2017 [cited 2021 Apr 8]. p. 35–77. https://linkinghub.elsevier.
com/retrieve/pii/B9780444636652000023
55. Lepine C, Christianson L, Davidson J, Summerfelt S. Woodchip bioreactors as treatment for recirculat-
ing aquaculture systems’ wastewater: A cost assessment of nitrogen removal. Aquac Eng [Internet].
2018 Nov [cited 2020 May 4]; 83:85–92. Available from: https://linkinghub.elsevier.com/retrieve/pii/
S0144860918300840
56. Robertson AI, Phillips MJ. Mangroves as filters of shrimp pond effluent: predictions and biogeochemi-
cal research needs. Hydrobiologia [Internet]. 1995 Jan [cited 2020 Mar 30]; 295(1–3):311–21. Avail-
able from: http://link.springer.com/10.1007/BF00029138
57. Tilley DR, Badrinarayanan H, Rosati R, Son J. Constructed wetlands as recirculation filters in large-
scale shrimp aquaculture. Aquac Eng [Internet]. 2002 Jun [cited 2020 Apr 1]; 26(2):81–109. Available
58. Lin YF, Jing SR, Lee DY, Chang YF, Chen YM, Shih KC. Performance of a constructed wetland
treating intensive shrimp aquaculture wastewater under high hydraulic loading rate. Environ Pollut
[Internet]. 2005 Apr [cited 2020 Apr 1]; 134(3):411–21. Available from: https://linkinghub.elsevier.
com/retrieve/pii/S0269749104003872 https://doi.org/10.1016/j.envpol.2004.09.015 PMID:
15620586
59. Bosma RH, Nguyen TH, Siahainenia AJ, Tran HTP, Tran HN. Shrimp-based livelihoods in mangrove
silvo-aquaculture farming systems. Rev Aquac [Internet]. 2016 Mar [cited 2020 Jun 24]; 8(1):43–60.
Available from: http://doi.wiley.com/10.1111/raq.12072

60. Jones AB, Preston NP. Sydeny rock oyster, Saccostrea commercialis (Iredale & Roughley), filtration
of shrimp farm effluent: the effects on water quaity. Aquac Res [Internet]. 1999 Jan [cited 2020 Jun 3];
30(1):51–7. Available from: http://doi.wiley.com/10.1046/j.1365-2109.1999.00299.x
61. Tom AP, Jayakumar JS, Biju M, Somarajan J, Ibrahim MA. Aquaculture wastewater treatment
technologies and their sustainability: A review. Energy Nexus [Internet]. 2021 Dec [cited 2023
Jan 11]; 4:100022. Available from: https://linkinghub.elsevier.com/retrieve/pii/
S277242712100022X
62. Astiyani WP, Prama EA, Akbarurrasyid M, Prabowo G, Sudinno D, Sha M. An Economic Analysis
Ecoshrimp White Shrimp (Litopenaeus vannamei) Concept on Shrimp Culture with Plastic Pond, Indo-
nesia. Aquac Indones. 2020; 7.
63. ASC. ASC Shrimp Standard Version 1.1. Aquaculture Stewardship Council; 2019.
64. BAP. Aquaculture Facility Certification: BAP Farm Standard. Global Aquaculture Alliance Best Aqua-
culture Practices; 2021.
65. Suantika G, Situmorang ML, Kurniawan JB, Pratiwi SA, Aditiawati P, Astuti DI, et al. Development of
a zero water discharge (ZWD)–Recirculating aquaculture system (RAS) hybrid system for super
intensive white shrimp (Litopenaeus vannamei) culture under low salinity conditions and its industrial
trial in commercial shrimp urban farming in Gresik, East Java, Indonesia. Aquac Eng. 2018 Aug;
82:12–24.
66. Christianson LE, Schipper LA. Moving Denitrifying Bioreactors beyond Proof of Concept: Introduction
to the Special Section. J Environ Qual [Internet]. 2016 May [cited 2020 Jun 8]; 45(3):757–61. Available
from: http://doi.wiley.com/10.2134/jeq2016.01.0013 https://doi.org/10.2134/jeq2016.01.0013 PMID:
27136139
67. Ramos R, Vinatea L, Seiffert W, Beltrame E, Silva JS, Costa RHR da. Treatment of shrimp effluent by
sedimentation and oyster filtration using Crassostrea gigas and C. rhizophorae. Braz Arch Biol Tech-
nol [Internet]. 2009 Jun [cited 2021 Feb 18]; 52(3):775–83. Available from: http://www.scielo.br/scielo.
php?script=sci_arttext&pid=S1516-89132009000300030&lng=en&tlng=en
68. Kohan A, Nasrolahi A, Aeinjamshid K, H. Kiabi B. Nutrient removal from aquaculture effluent using set-
tling ponds and filter-feeding species (Amphibalanus amphitrite and Saccostrea cucullata): an in-situ
study. Iran J Fish Sci [Internet]. 2018 Dec [cited 2020 Sep 17];(Online First). Available from: http://doi.
org/10.22092/ijfs.2018.117925
69. Primavera JH, Altamirano JP, Lebata MJHL, delos Reyes AA Jr., Pitogo CL. MANGROVES AND
SHRIMP POND CULTURE EFFLUENTS IN AKLAN, PANAY IS., CENTRAL PHILIPPINES. Bull Mar
Sci. 2007; 80(3):11.
70. Hargan KE, Williams B, Nuangsaeng B, Siriwong S, Tassawad P, Chaiharn C, et al. Understanding
the fate of shrimp aquaculture effluent in a mangrove ecosystem: Aiding management for coastal con-
servation. Macinnis-Ng C, editor. J Appl Ecol [Internet]. 2020 Apr [cited 2023 Jan 24]; 57(4):754–65.
Available from: https://onlinelibrary.wiley.com/doi/10.1111/1365-2664.13579
71. Stefanakis AI. Constructed Wetlands for Industrial Wastewater Treatment. First. West Sussex, UK:
John Wiley & Sons, Ltd; 2018.
72. Davidson J, Helwig N, Summerfelt ST. Fluidized sand biofilters used to remove ammonia, biochemical
oxygen demand, total coliform bacteria, and suspended solids from an intensive aquaculture effluent.
Aquac Eng [Internet]. 2008 Aug [cited 2020 Jun 9]; 39(1):6–15. Available from: https://linkinghub.
73. MAT Filtration Technologies. Equipment Imperial Specification & Price List. 2019.
74. Li X, Deng Y, Li X, Ma X, Wang J, Li J. Integration of Marine Macroalgae (Chaetomorpha maxima) with
a Moving Bed Bioreactor for Nutrient Removal from Maricultural Wastewater. Archaea [Internet]. 2020
Jun 23 [cited 2021 Dec 3]; 2020:1–13. Available from: https://www.hindawi.com/journals/archaea/
2020/8848120/
75. Christianson LE, Lepine C, Sharrer KL, Summerfelt ST. Denitrifying bioreactor clogging potential dur-
ing wastewater treatment. Water Res [Internet]. 2016 Nov [cited 2020 Jun 8]; 105:147–56. Available
from: https://linkinghub.elsevier.com/retrieve/pii/S0043135416306765 https://doi.org/10.1016/j.
watres.2016.08.067 PMID: 27614035
76. Sharrer KL, Christianson LE, Lepine C, Summerfelt ST. Modeling and mitigation of denitrification
‘woodchip’ bioreactor phosphorus releases during treatment of aquaculture wastewater. Ecol Eng
[Internet]. 2016 Aug [cited 2020 Jun 11]; 93:135–43. Available from: https://linkinghub.elsevier.com/
retrieve/pii/S0925857416302464
77. Choudhury T, Robertson WD, Finnigan DS. Suspended Sediment and Phosphorus Removal in a
Woodchip Filter System Treating Agricultural Wash Water. J Environ Qual [Internet]. 2016 May [cited
2021 Feb 18]; 45(3):796–802. Available from: http://doi.wiley.com/10.2134/jeq2015.07.0380 https://
doi.org/10.2134/jeq2015.07.0380 PMID: 27136144

78. Lepine C, Christianson L, McIsaac G, Summerfelt S. Denitrifying bioreactor inflow manifold design for
treatment of aquacultural wastewater. Aquac Eng [Internet]. 2020 Feb [cited 2020 Jun 17]; 88:102036.
Available from: https://linkinghub.elsevier.com/retrieve/pii/S0144860919301402
79. Bondurant JA, Brockway CE, Brown MJ. SOME ASPECTS OF SEDIMENTATION POND DESIGN.
Haan CT Ed Proc NAtl Symp Urban Hydrol Sediment Control. 1975;C/35-C/45.
80. Engle CR, Valderrama D. Farm-level costs of settling basins for treatment of effluents from levee-style
catfish ponds. Aquac Eng [Internet]. 2003 Aug [cited 2020 Jun 9]; 28(3–4):171–99. Available from:
https://linkinghub.elsevier.com/retrieve/pii/S014486090300027X
81. Boyd CE. Settling Basin Desing, Operation. 2012. Settling basin design, operation. https://www.
globalseafood.org/advocate/settling-basin-design-operation/
82. Rose JM, Bricker SB, Ferreira JG. Comparative analysis of modeled nitrogen removal by shellfish
farms. Mar Pollut Bull [Internet]. 2015 Feb [cited 2020 Oct 6]; 91(1):185–90. Available from: https://
linkinghub.elsevier.com/retrieve/pii/S0025326X14008078 https://doi.org/10.1016/j.marpolbul.2014.
12.006 PMID: 25534625
83. Soto D, editor. Integrated mariculture: a global review. Rome: Food and Agriculture Organization of
the United Nations; 2009. 183 p. (FAO fisheries and aquaculture technical paper).
84. Samocha TM, Fricker J, Ali AM, Shpigel M, Neori A. Growth and nutrient uptake of the macroalga Gra-
cilaria tikvahiae cultured with the shrimp Litopenaeus vannamei in an Integrated Multi-Trophic Aqua-
culture (IMTA) system. Aquaculture [Internet]. 2015 Sep [cited 2020 Jun 10]; 446:263–71. Available
85. Ferreira JG, Hawkins AJS, Bricker SB. Management of productivity, environmental effects and profit-
ability of shellfish aquaculture—the Farm Aquaculture Resource Management (FARM) model. Aqua-
culture [Internet]. 2007 Apr [cited 2021 Mar 2]; 264(1–4):160–74. Available from: https://linkinghub.
86. Ahmed N, Thompson S, Glaser M. Integrated mangrove-shrimp cultivation: Potential for blue car-
bon sequestration. Ambio [Internet]. 2017 Oct 4 [cited 2019 Oct 14]; Available from: http://link.
springer.com/10.1007/s13280-017-0946-2 https://doi.org/10.1007/s13280-017-0946-2 PMID:
28980188
87. McIlveen S, Hung PQ. Improving livelihoods and increasing coastal resilience: A look at integrated
mangrove-shrimp aquaculture in Vietnam. Aquaculture Asia. 2019; 23(4):4.
88. Langergraber G, Dotro G, Nivala J, Rizzo A, Stein OR, editors. Wetland Technology: Practical Infor-
mation on the Design and Application of Treatment Wetlands [Internet]. London, UK: IWA Publishing;
2020 [cited 2021 Feb 26]. (Scientific and Technical Report). http://iwaponline.com/ebooks/book/780/
Wetland-Technology-Practical-Information-on-the
89. Wu Y, Chung A, Tam NFY, Pi N, Wong MH. Constructed mangrove wetland as secondary treatment
system for municipal wastewater. Ecol Eng [Internet]. 2008 Sep [cited 2020 May 4]; 34(2):137–46.
Available from: https://linkinghub.elsevier.com/retrieve/pii/S092585740800147X
90. Yang Q, Tam NFY, Wong YS, Luan TG, Su WS, Lan CY, et al. Potential use of mangroves as con-
structed wetland for municipal sewage treatment in Futian, Shenzhen, China. Mar Pollut Bull. 2008; 9.
https://doi.org/10.1016/j.marpolbul.2008.01.037 PMID: 18342338
91. Tam NFY, Tin TT, Wong YS. Performance of a 10-Year Constructed Mangrove Wetland forWaste-
water Treatment. In 2018 [cited 2020 Sep 17]. http://avestia.com/CSEE2018_Proceedings/files/paper/
AWSPT/AWSPT_108.pdf
92. Twilley RR, Day JW Jr., editors. Mangrove Wetlands. In: Estuarine Ecology [Internet]. Hoboken, NJ,
USA: John Wiley & Sons, Inc.; 2012 [cited 2020 Oct 30]. p. 165–202. Available from: http://doi.wiley.
com/10.1002/9781118412787.ch7
93. Ahmad T, Tjaronge M, Cholik F. THE USE OF MANGROVE STANDS FOR SHRIMP POND WASTE-
WATER TREATMENT. Indones Fish Res J [Internet]. 2001 Jun 5 [cited 2020 May 8]; 7(1):7. Available
from: http://ejournal-balitbang.kkp.go.id/index.php/ifrj/article/view/5589
94. Osman M, Wan Yusof K, Takaijudin H, Goh HW, Abdul Malek M, Azizan NA, et al. A Review of Nitro-
gen Removal for Urban Stormwater Runoff in Bioretention System. Sustainability [Internet]. 2019
Sep 30 [cited 2021 Jun 7]; 11(19):5415. Available from: https://www.mdpi.com/2071-1050/11/19/
5415
95. Gunawardena M, Rowan JS. Economic Valuation of a Mangrove Ecosystem Threatened by Shrimp
Aquaculture in Sri Lanka. Environ Manage [Internet]. 2005 Oct [cited 2021 Apr 19]; 36(4):535–50.
Available from: http://link.springer.com/10.1007/s00267-003-0286-9 https://doi.org/10.1007/s00267-
003-0286-9 PMID: 16151655
96. Barrington K, Chopin T, Robinson S. Integrated multi-trophic aquaculture (IMTA) in marine temperate
waters. In: Integrated mariculture: a global review. Rome, FAO: FAO Fisheries Technical Paper;
2009. p. 7–46.

97. Steer D, Aseltyne T, Fraser L. Life-cycle economic model of small treatment wetlands for domestic
wastewater disposal. Ecol Econ [Internet]. 2003 Mar [cited 2021 Apr 19]; 44(2–3):359–69. Available
from: https://linkinghub.elsevier.com/retrieve/pii/S092180090300003X
98. Hakim LL, Groeneveld R, Bosma R. Cost-Benefit-Analysis (CBA) on Improving Aquaculture and
Restoring Mangrove in Indonesia. 2018 Jul; Wageningen University and Research.
99. Smith G, Cooley D, Brown B, Fritriana R, Hyman E. Cost-Benefit Analysis of Mangrove Conservation
Versus Shrimp Aquaculture in Bintuni Bay and Mimika, Indonesia. Washington, D.C: Crown Agents
USA and Abt Associates; 2020.
100. Lummer SL. Equivalent Real Annual Costs: Evaluating Investment Alternatives with Unequal Lives
Under. Eng Econ [Internet]. 1986 Jan [cited 2021 Apr 9]; 31(4):317–26. Available from: http://www.
tandfonline.com/doi/abs/10.1080/00137918608902947
101. Ruiz Campo S, Zuniga-Jara S. Reviewing capital cost estimations in aquaculture. Aquac Econ Manag
[Internet]. 2018 Jan 2 [cited 2021 Apr 9]; 22(1):72–93. Available from: https://www.tandfonline.com/
doi/full/10.1080/13657305.2017.1300839
102. JALA Tech. JALA Shrimp Price Portal [Internet]. 2021. https://app.jala.tech/harga_udang
103. BAP. Aquaculture Facility Certification: finfish and Crustacean Farms Certification Standards, Guide-
lines. Best Aquaculture Practices; 2017.
104. Ecosystems and human well-being: synthesis. Washington, DC: Island Press; 2005.
105. Ramsar Convention on Wetlands. Global Wetland Outlook: State of the world’s wetlands and their ser-
vices to people 2018. Gland, Switzerland: Ramsar Convention Secretariat; 2018 p. 88.
106. Ebeling JM, Vinci B. Solids Capture: Recirculating Aquaculture Systems Short Course [Internet]. Uni-
versity of Arizona. https://cals.arizona.edu/azaqua/ista/ISTA7/RecircWorkshop/Workshop%20PP%
20%20%26%20Misc%20Papers%20Adobe%202006/5%20Solids%20Capture/Solids%20Control.pdf
107. Tantu AG, Salam S, Ishak M. Vaname Shrimp Cultivation (Litopenaeus vannamei) on High Stocking
Densities in Controlled Ponds. J Aquac Res Dev. 2020; 11(583):6.
108. Rivera-Monroy VH, Torres LA, Bahamon N, Newmark F, Twilley RR. The Potential Use of Mangrove
Forests as Nitrogen Sinks of Shrimp Aquaculture Pond Effluents: The Role of Denitrification. J World
Aquac Soc [Internet]. 1999 Mar [cited 2020 Oct 7]; 30(1):12–25. Available from: http://doi.wiley.com/
10.1111/j.1749-7345.1999.tb00313.x
109. Teichert-Coddington DR, Martinez D, Ramı́rez E. Partial nutrient budgets for semi-intensive shrimp
farms in Honduras. Aquaculture [Internet]. 2000 Oct [cited 2020 May 22]; 190(1–2):139–54. Available
110. Sun W, Boyd CE. Phosphorus and Nitrogen Budgets for Inland, Saline Water Shrimp Ponds in Ala-
bama. Fish Aquac J [Internet]. 2013 [cited 2020 Jul 1]; 04(02). Available from: https://www.
omicsonline.com/open-access/phosphorus-and-nitrogen-budgets-for-inland-saline-water-shrimp-
ponds-in-alabama-2150-3508.1000080.php?aid=21098
111. Davis RP, Boyd CE. A comparison of the technical efficiency of Aquaculture Stewardship Council certi-
fied shrimp farms to non-certified farms. Curr Res Environ Sustain [Internet]. 2021 [cited 2022 Jan 3];
3:100069. Available from: https://linkinghub.elsevier.com/retrieve/pii/S2666049021000451
112. DCLG. Multi-criteria analysis: a manual. Wetherby: Department fro Communities and Local Govern-
ment; 2009. Report No.: 08ACST05703.
113. Campanati C, Willer D, Schubert J, Aldridge DC. Sustainable Intensification of Aquaculture through
Nutrient Recycling and Circular Economies: More Fish, Less Waste, Blue Growth. Rev Fish Sci Aquac
[Internet]. 2021 Mar 17 [cited 2022 Jan 5];1–50. Available from: https://www.tandfonline.com/doi/full/
10.1080/23308249.2021.1897520
114. Emerenciano MGC, Martı́nez-Córdova LR, Martı́nez-Porchas M, Miranda-Baeza A. Biofloc Technol-
ogy (BFT): A Tool for Water Quality Management in Aquaculture. In: Tutu H, editor. Water Quality
[Internet]. InTech; 2017 [cited 2020 Jun 8]. http://www.intechopen.com/books/water-quality/biofloc-
technology-bft-a-tool-for-water-quality-management-in-aquaculture
115. Kumar V, Roy S, Meena DK, Sarkar UK. Application of Probiotics in Shrimp Aquaculture: Importance,
Mechanisms of Action, and Methods of Administration. Rev Fish Sci Aquac [Internet]. 2016 Oct 1; 24
(4):342–68. Available from: https://doi.org/10.1080/23308249.2016.1193841
116. Joffre OM, Klerkx L, Khoa TND. Aquaculture innovation system analysis of transition to sustainable
intensification in shrimp farming. Agron Sustain Dev [Internet]. 2018 Jun 11; 38(3):34. Available from:
https://doi.org/10.1007/s13593-018-0511-9
117. Kittinger JN, Bernard M, Finkbeiner E, Murphy E, Obregon P, Klinger DH, et al. Applying a jurisdic-
tional approach to support sustainable seafood. Conserv Sci Pract [Internet]. 2021 Mar 4 [cited 2021
Mar 5]; Available from: https://onlinelibrary.wiley.com/doi/10.1111/csp2.386

118. Tepe Y, Temel FA. Treatment of Effluents from Fish and Shrimp Aquaculture in Constructed Wetlands.
In: Constructed Wetlands for Industrial Wastewater Treatment. First. John Wiley & Sons, Ltd; 2018. p.
105–44.
119. Ross LG, Telfer TC, Falconer L, Soto D, Aguilar-Manjarrez J, Ashmah R, et al. Carrying capacities and
site selection within the ecosystem approach to aquaculture. In: Site seslection and carrying capacities
for inland and coastal aquaculture. Rome, FAO: FAO/Institute of Aquaculture, Univerity of Stirling;
2013. p. 19–46.
120. Rubel H, Woods W, Pérez D, Unnikrishnan S, Zielcke S, Lidy C, et al. A Strategic Approach to Sustain-
able Shrimp Production in Thailand: The case for impoved economics and sustainability. Boston Con-
sulting Group; 2019 Jul. Report No.: Thailand.
Approach to Sustainable Shrimp Production in Vietnam: The case for improved economics and sus-
tainability. Boston Consulting Group; 2019 Aug. Report No.: Vietnam.
Approach to Sustainable Shrimp Production in India: The case for improved economics and sustain-
ability. Boston Consulting Group; 2020 Jan. Report No.: India.
123. Lewis RR, Brown B. Ecological Mangrove Rehabiliation. A Field Manual for Practitioners. Canadian
International Development Agency and OXFAM; 2014.
124. Bayraktarov E, Saunders MI, Abdullah S, Mills M, Beher J, Possingham HP, et al. The cost and feasi-
bility of marine coastal restoration. Ecol Appl [Internet]. 2016 Jun [cited 2021 Feb 10]; 26(4):1055–74.
Available from: http://doi.wiley.com/10.1890/15-1077 https://doi.org/10.1890/15-1077 PMID:
27509748
125. Zhang DQ, Jinadasa KBSN, Gersberg RM, Liu Y, Tan SK, Ng WJ. Application of constructed wetlands
for wastewater treatment in tropical and subtropical regions (2000–2013). J Environ Sci [Internet].
2015 Apr [cited 2020 Sep 25]; 30:30–46. Available from: https://linkinghub.elsevier.com/retrieve/pii/
S1001074215000595 https://doi.org/10.1016/j.jes.2014.10.013 PMID: 25872707
126. AIMS. Mixed Shrimp Farming-Mangrove Forestry Model in the Mekong Delta. Australian Institute of
Marins Science; 1999 Jun. Report No.: Project PN9412.
127. International Conservation. VIDA MANGLAR Impact Report. Arlington, VA: Conservation Interna-
tional; 2022 p. 10.
128. Shimoda T, Fujioka Y, Srithong C, Aryuthaka C. Phosphorus budget in shrimp aquaculture pond with
mangrove enclosure and aquaculture performance. Fish Sci [Internet]. 2005 Dec [cited 2020 Jun 18];
71(6):1249–55. Available from: http://link.springer.com/10.1111/j.1444-2906.2005.01090.x
129. Anh PT, Kroeze C, Bush SR, Mol APJ. Water pollution by intensive brackish shrimp farming in south-
east Vietnam: Causes and options for control. Agric Water Manag [Internet]. 2010 Jun [cited 2021 Mar
1]; 97(6):872–82. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0378377410000363
130. Lin YF, Jing SR, Lee DY, Chang YF, Sui HY. Constructed Wetlands for Water Pollution Management
of Aquaculture Farms Conducting Earthen Pond Culture. Water Environ Res [Internet]. 2010 Aug
[cited 2020 Sep 21]; 82(8):759–68. Available from: http://doi.wiley.com/10.2175/
106143010X12609736966685 https://doi.org/10.2175/106143010x12609736966685 PMID:
20853755
131. Aslan A, Rahman AF, Robeson SM, Ilman M. Land-use dynamics associated with mangrove defores-
tation for aquaculture and the subsequent abandonment of ponds. Sci Total Environ [Internet]. 2021
Oct [cited 2021 Jul 1]; 791:148320. Available from: https://linkinghub.elsevier.com/retrieve/pii/
S004896972103391X https://doi.org/10.1016/j.scitotenv.2021.148320 PMID: 34126482
132. The Global Innovation Lab for Climate Finance. Climate Smart Shrimp Fund. 2022. Climate Smart
Shrimp Fund. https://www.climatefinancelab.org/project/climate-smart-shrimp-fund/
133. de Groot R, Brander L, Solomonides S. Update of global ecosystem service valuation database
(ESVD). Wageningen, The Netherlands: Foundation for Sustainable Development; 2020 p. 58.
Report No.: FSD Report No 2020–06.
134. Khan SU, Liu G, Zhao M, Chien H, Lu Q, Khan AA, et al. Spatial prioritization of willingness to pay for
ecosystem services. A novel notion of distance from origin’s impression. Environ Sci Pollut Res [Inter-
net]. 2020 Jan [cited 2021 Jul 6]; 27(3):3100–12. Available from: http://link.springer.com/10.1007/
s11356-019-06538-4 https://doi.org/10.1007/s11356-019-06538-4 PMID: 31838703
135. Small N, Munday M, Durance I. The challenge of valuing ecosystem services that have no material
benefits. Glob Environ Change [Internet]. 2017 May [cited 2021 Jun 23]; 44:57–67. Available from:
https://linkinghub.elsevier.com/retrieve/pii/S0959378017303540
136. Sampantamit T, Ho L, Lachat C, Sutummawong N, Sorgeloos P, Goethals P. Aquaculture Production
and Its Environmental Sustainability in Thailand: Challenges and Potential Solutions. Sustainability

[Internet]. 2020 Mar 5 [cited 2021 Mar 2]; 12(5):2010. Available from: https://www.mdpi.com/2071-
1050/12/5/2010
137. Valiela I, Bowen JL, York JK. Mangrove Forests: One of the World’s Threatened Major Tropical Envi-
ronments. BioScience [Internet]. 2001 [cited 2020 Oct 23]; 51(10):807. Available from: https://
academic.oup.com/bioscience/article/51/10/807-815/245210
138. Richards DR, Thompson BS, Wijedasa L. Quantifying net loss of global mangrove carbon stocks from
20 years of land cover change. Nat Commun [Internet]. 2020 Dec [cited 2020 Oct 23]; 11(1):4260.
Available from: http://www.nature.com/articles/s41467-020-18118-z https://doi.org/10.1038/s41467-
020-18118-z PMID: 32848150
139. Liu S, Li X, Chen D, Duan Y, Ji H, Zhang L, et al. Understanding Land use/Land cover dynamics and
impacts of human activities in the Mekong Delta over the last 40 years. Glob Ecol Conserv [Internet].
2020 Jun [cited 2020 Dec 17]; 22:e00991. Available from: https://linkinghub.elsevier.com/retrieve/pii/
S2351989419308674
140. Sun H, He Z, Zhang M, Yen L, Cao Y, Hu Z, et al. Spatial variation of soil properties impacted by aqua-
culture effluent in a small-scale mangrove. Mar Pollut Bull [Internet]. 2020 Nov [cited 2020 Sep 25];
160:111511. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0025326X20306299 https://
doi.org/10.1016/j.marpolbul.2020.111511 PMID: 32861934
141. Tian Y, Chen G, Lu H, Zhu H, Ye Y. Effects of shrimp pond effluents on stocks of organic carbon, nitro-
gen and phosphorus in soils of Kandelia obovata forests along Jiulong River Estuary. Mar Pollut Bull
[Internet]. 2019 Dec [cited 2022 Jan 6]; 149:110657. Available from: https://linkinghub.elsevier.com/
retrieve/pii/S0025326X19308057
142. Wang D, Xie X, Tang W, Pan H, Luo J. Suitability of Nansha Mangrove Wetland for High Nitrogen
Shrimp Pond Wastewater Treatment. Bull Environ Contam Toxicol [Internet]. 2021 Feb [cited 2022
Jan 6]; 106(2):349–54. Available from: http://link.springer.com/10.1007/s00128-020-03060-z https://
doi.org/10.1007/s00128-020-03060-z PMID: 33258968
143. Queiroz HM, Ferreira TO, Taniguchi CAK, Barcellos D, do Nascimento JC, Nóbrega GN, et al. Nitro-
gen mineralization and eutrophication risks in mangroves receiving shrimp farming effluents. Environ
Sci Pollut Res [Internet]. 2020 Oct [cited 2022 Jan 6]; 27(28):34941–50. Available from: https://link.
springer.com/10.1007/s11356-020-09720-1 https://doi.org/10.1007/s11356-020-09720-1 PMID:
32583107
144. Barcellos D, Queiroz HM, Nóbrega GN, de Oliveira Filho RL, Santaella ST, Otero XL, et al. Phospho-
rus enriched effluents increase eutrophication risks for mangrove systems in northeastern Brazil. Mar
Pollut Bull [Internet]. 2019 May [cited 2020 Jun 24]; 142:58–63. Available from: https://linkinghub.
elsevier.com/retrieve/pii/S0025326X19302152 https://doi.org/10.1016/j.marpolbul.2019.03.031
PMID: 31232342
145. Green-Gray Community of Practice. Practical Guide to Implementing Green-Gray Infrastructure [Inter-
net]. Conservation International; 2020 p. 1–172. https://www.conservation.org/docs/default-source/
publication-pdfs/ci-green-gray-practical-guide-v07.pdf?sfvrsn=3cc5cf18_4
146. Winterwerp JC, Albers T, Anthony EJ, Friess DA, Mancheño AG, Moseley K, et al. Managing erosion
of mangrove-mud coasts with permeable dams—lessons learned. Ecol Eng [Internet]. 2020 Dec [cited
2020 Dec 1]; 158:106078. Available from: https://linkinghub.elsevier.com/retrieve/pii/
S0925857420303669
147. Mitchell T, Maxwell S. Defining climate compatible development [Internet]. Climate & Development Knowl-
edge Network; 2010. https://cdkn.org/wp-content/uploads/2012/10/CDKN-CCD-Planning_english.pdf
148. Harkes IHT, Drengstig A, Kumara MP, Jayasinghe JMPK, Huxham M. Shrimp aquaculture as a vehicle
for Climate Compatible Development in Sri Lanka. The case of Puttalam Lagoon. Mar Policy [Internet].
2015 Nov [cited 2020 Jun 24]; 61:273–83. Available from: https://linkinghub.elsevier.com/retrieve/pii/
S0308597X15002225
149. Tam NFY, shan Wong Y. Constructed Wetland with Mixed Mangrove and Non-mangrove plants for
municpal Sewage Treatment. Int Proc Chem Biol Environ Eng. 2014; 61(11):60–3.
150. Gautier D, Amador J, Newmark F. The use of mangrove wetland as a biofilter to treat shrimp pond
effluents: preliminary results of an experiment on the Caribbean coast of Colombia. Aquac Res [Inter-
net]. 2001 Oct [cited 2020 May 8]; 32(10):787–99. Available from: http://doi.wiley.com/10.1046/j.1365-
2109.2001.00614.x
151. Zhang JE, Liu JL, Ouyang Y, Liao BW, Zhao BL. Removal of nutrients and heavy metals from waste-
water with mangrove Sonneratia apetala Buch-Ham. Ecol Eng [Internet]. 2010 Jun [cited 2020 May 4];
36(6):807–12. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0925857410000601

Journal PSTR 0000076

Uploaded by

Copyright:

Available Formats

Journal PSTR 0000076

Uploaded by

Document Information

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Journal PSTR 0000076

Uploaded by

Copyright:

Available Formats

PLOS SUSTAINABILITY AND TRANSFORMATION

A nature-based solutions approach to

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 1 / 32

Competing interests: I have read the journal’s

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 2 / 32

Table 1. Whiteleg shrimp (Litopenaeus vannamei) production intensities and characteristics.

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 3 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 4 / 32

Materials and methods

Evaluated treatment systems

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 5 / 32

Data collection and analysis

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 6 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 7 / 32

production scenarios to model TN and TP effluent waste loads. Generalized production

Table 3. Production parameters and assumptions for modelled scenarios [17,34].

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 8 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 9 / 32

EAC is described in (Eq 5) as:

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 10 / 32

Zi ¼ j1 ðXi Xmax 1 Þj ð8Þ

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 11 / 32

Treatment system performance

Water quality criteria

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 12 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 13 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 14 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 15 / 32

* Indicates modelled scenarios and outputs from this study.

Equivalent annual costs per kg

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 16 / 32

Normalization and aggregation of performance indicators

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 17 / 32

Estimated nutrient loading

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 18 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 19 / 32

Water quality criteria

Equivalent annual costs per kg and financial considerations

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 20 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 21 / 32

Ecosystem services and benefits to the environment

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 22 / 32

Areas for further research

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 23 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 24 / 32

5. Le Gouvello R, Brugère C, Simard F. Aquaculture and Nature-based Solutions: identifying synergies

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 25 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 26 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 27 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 28 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 29 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 30 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 31 / 32

PLOS Sustainability and Transformation | https://doi.org/10.1371/journal.pstr.0000076 August 30, 2023 32 / 32

You might also like