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Aquaculture in coastal urbanized areas: A
comparative review of the challenges posed by
Harmful Algal Blooms
Aurore Trottet, Christaline George, Guillaume Drillet & Federico M. Lauro
To cite this article: Aurore Trottet, Christaline George, Guillaume Drillet & Federico M. Lauro
(2021): Aquaculture in coastal urbanized areas: A comparative review of the challenges posed
by Harmful Algal Blooms, Critical Reviews in Environmental Science and Technology, DOI:
10.1080/10643389.2021.1897372
To link to this article: https://doi.org/10.1080/10643389.2021.1897372
© 2021 The Author(s). Published with
license by Taylor & Francis Group, LLC
Published online: 17 Mar 2021.
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Aquaculture in coastal urbanized areas: A comparative
review of the challenges posed by Harmful
Algal Blooms
Aurore Trottet
a
, Christaline George
b
, Guillaume Drillet
c
, and
Federico M. Lauro
b,d
a
DHI Water & Environment(s) Pte Ltd, Singapore, Singapore;
b
Asian School of the Environment,
Nanyang Technological University, Singapore, Singapore;
c
SGS Testing & Control Services
Singapore Pte Ltd, Singapore, Singapore;
d
Singapore Centre for Environmental Life Sciences
Engineering (SCELSE), Nanyang Technological University, Singapore, Singapore
ABSTRACT
Increasing global population has
resulted in increased urbanization
of coastal areas across the globe.
Such an increase generates many
challenges for sustainable food
production and food security. The
development of aquaculture has
proven to be an extremely good
option to ensure food security
(uninterrupted supply and good
quality of food) by many coun-
tries, especially those with urban
areas affected by space limita-
tions such as Singapore. However, the implementation of aquaculture is not without its
challenges and impacts to the environment, with Harmful Algal Blooms (HABs) being
one of the major concerns in coastal waters. In this review we analyze the development
of the aquaculture industry with respect to HABs in Singapore and compare it to similar
urban areas such as Hong Kong (SAR China), Salalah (Oman), Cape Town (South Africa),
Valencia (Spain), Rotterdam (The Netherlands), Tampa bay (USA), Vancouver (Canada),
and Sydney (Australia). Along with HABs, the abovementioned urban areas face different
challenges in sustainably increasing their aquaculture production with respect to the
economy and geography. This review further assesses the different production and mon-
itoring strategies that have been implemented to counter these challenges while sus-
tainably increasing production. The ongoing COVID-19 pandemic has affected the world
with lockdowns and border closures resulting in logistical difficulties in seafood trade
which has further accentuated the dependencies on food import. We conclude that the
challenges faced by urban areas for sustainable achievement of food security through
development of the aquaculture industry can be effectively managed through proper
planning, management and collaboration of knowledge/skills on an international level.
KEYWORDS HABs; urbanization; aquaculture; food security; mitigation; Singapore
ß2021 The Author(s). Published with license by Taylor & Francis Group, LLC
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives
License (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial re-use, distribution, and reproduction
in any medium, provided the original work is properly cited, and is not altered, transformed, or built upon in any way.
CONTACT Federico M. Lauro flauro@ntu.edu.sg Asian School of the Environment, Nanyang Technological
University, Singapore, Singapore.
These authors contributed equally to this work.
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY
https://doi.org/10.1080/10643389.2021.1897372
Introduction
The United Nations (UN) has projected that the world population would
increase from 7.7 billion in 2019 to 9.7 billion by 2050 (UN, 2019). To
date, it is estimated that 55% of the world’s current population lives in
urban areas (UN, 2018). Despite low levels of urbanization, Asia is home
to 54% of the world’s urban population, followed by Europe and Africa
with 13% each (UN, 2018). The projected increase in the world’s total
population combined with that of urbanization could add another 2.5 bil-
lion people to urban areas by 2050, with close to 90% of this increase tak-
ing place in Asia and Africa (UN, 2020).
This increase in population will require a concurrent increase in food
production. The global aquaculture sector expects productions to increase
by over 50% to meet global food demands in the next two decades and this
needs to be done in an economically, socially and environmentally sustain-
able manner. In all respects, an aquaculture dominant food production eco-
system to meet future demand is desirable because of its limited impacts
on deforestation and land use in general (Froehlich et al., 2018). Yet, the
expansion of aquaculture in both northern and southern hemispheres has
been associated with environmental issues of harmful algal blooms (HABs)
leading to indiscriminate killings of aquatic organisms, closure of beaches
and restriction of recreational activities (Anderson et al., 2012). The defin-
ition of HABs in the context of this review is adopted from Hallegraeff
et al. (2004) and includes i) the proliferation of microalgae to high biomass
causing harmless water discolorations but indiscriminate killings of marine
organisms through oxygen depletion; ii) the proliferation of microalgae to
high biomass, nontoxic to humans but killing fish and invertebrates
through mechanical damage or clogging of their gills and iii) the produc-
tion of toxins by microalgae harmful for marine organisms and for humans
by transfer through the food chain and physical contact.
HABs in the past forty years have increased in frequency, intensity and
geographical distribution (Dale & Yentsch, 1978; Heisler et al., 2008,
Hallegraeff, 2010; Anderson et al., 2012; Lin et al., 2020). The increase of
such events is not always well understood and has been attributed to differ-
ent factors that can increase the amount of nutrients into the water such as
discharge from waste-water treatment plants, shipping, oil-refinaries, tour-
ism, port- activities, housing, deslination plants, coastal farms and aquacul-
ture (Figure 1; Trottet et al., 2018). Figure 1 shows two-way interactions in
the case of desalination plants, coastal farms and aquaculture farms which
can stimulate HAB events, but can also be affected by HABs resulting in
clogging of the filters in desalination plants and killing of fish stocks. In
2 A. TROTTET ET AL.
addition to human activities that can stimulate HABs, natural climato-
logical factors such as seasonal changes can stimulate HABs too in some
areas (Al-Azri et al., 2013). Many of these HAB species are cosmopolitan
with serious negative impacts on the ecosystem, economies of the affected
areas and on public health as documented in the past HAB events across
the globe (Anderson et al., 2012).
HABs tremendously impact aquaculture resulting in devastating eco-
nomic losses locally or regionally and may even lead to a shortage of food
supply or retail of fish with compromised quality (FAO, 2020a). Food sup-
ply and quality are crucial aspects of food security which has become an
increasing global concern especially for developed countries which are
heavily dependent on food imports. These food imports can further be
affected by political unrest, conflict and wars between nations, diseases and
epidemics such as the ongoing COVID-19 and other factors which have led
many nations to adopt strategies to improve their food security measures.
Such measures should be centered on the development of technological
advancements to improve self-sufficiency and shorten supply chains,
thereby enabling sustainable aquaculture practices (Nat.Plants, 2020; Teng,
2020). The concept of sustainable aquaculture adopted in this review
Figure 1. A conceptual diagram showing the various coastal urban developments in the dis-
cussed urban areas, contribution of these processes to eutrophication and the occurrences of
HABs. Urban infrastructure such as desalination plants and aquaculture farms are represented
by a two-way arrow showing both their contribution to the development of HABs and also
how they can be impacted by HABs.
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 3
follows the FAO definition - “An ecosystem approach to aquaculture
(EAA) is a strategy for the integration of the activity within the wider eco-
system such that it promotes sustainable development, equity and resilience
of interlinked social-ecological systems”(FAO, 2010).
As majority of the urban infrastructure is expected to develop in Asia in
the next few years (Teng, 2020), many nations in this region could accom-
modate to this growth by protecting food security with sustainable develop-
ment of their aquaculture industry. This may become challenging for
knowledge-based economies in Asia such as Singapore. Located in
Southeast Asia, the city-state of Singapore is an island of 718.3 km2
bounded by the Straits of Johor in the north and the Straits of Singapore
in the South and characterized by a very dense population of 5,791,901
inhabitants and intense port activities (Table 1,Figures 2 and 3) (Gin et al.,
2006). With such dense population and limited space achieving self-pro-
duction becomes a challenge (Teng, 2020). However, the advantage that
Singapore has is the coastline which is being exploited to maximize the
urban infrastructure and aquaculture production potential. With such
rigorous coastal developments, increased nutrient discharges would inevit-
ably increase the risks of HAB occurrences and therefore their associated
negative impacts on the economy and food security objectives.
We review the situation in urban areas with similarities to Singapore
within countries located in every continent except Antarctica (i.e. urban
areas experiencing rapid coastal developments, having an emerging aquacul-
ture industry in a limited space). These urban areas along with Singapore
were reviewed on all key aspects of their water bodies, population, port
activities, and aquaculture production (Table 1). The chosen urban areas
include Hong Kong (SAR China), Salalah/Oman, Cape Town area (South
Africa), Valencia (Spain), Rotterdam (The Netherlands), Tampa bay (USA),
Vancouver area (Canada), and Sydney (Australia) (Figures 2 and 3). We rec-
ognize that the significance of the key aspects chosen for comparison differs
for the different urban areas. A record of HAB events for each urban area
with year, location, organisms involved, cause and characteristics with eco-
nomic and/or environmental losses are presented in Table 2 based on the
availability of these records. Therefore, we recognize that the information in
Table 2 may not be an exhaustive list as there may have been HAB events
which may not have been recorded. Mitigation and management measures
were also included when available (Table 2).
Singapore: a reference for sustainable ‘self-sufficiency’through aquaculture
Due to lack of natural resources such as land and water Singapore has tran-
sitioned from a fishing village in the 1950s to an urbanized, high-income
4 A. TROTTET ET AL.
Table 1. Description of cities being investigated with respect to their demographics, surrounding water bodies, port activity (in twenty-foot equivalent
units, TEUs) and ranking as well as aquaculture and fisheries production. Description of aquaculture activities is also included.
City (Country)
Region
(Water body)
Population
(hab.)
1
Port (10
3
TEUs) /
Rank
2
Aquaculture
production
(tonnes)
7
Fisheries
production
(tonnes)
7
Developing Aquaculture activities Reference
Singapore
(Singapore)
Asia (South
China Sea /
Pacific Ocean)
5,791,901 36,599 / 2 5,3351,418There are approximately 127
#
fish farms including
several land-based hatchery/culture farms. The fish
species produced are mostly groupers, seabass,
snappers and milkfish. Most coastal-based
aquaculture farms are in the Straits of Johor and use
open net cage systems to grow their fish. In the
Straits of Singapore, there is one open sea farm
producing Asian seabass. Local fish production in
2019 was estimated to 4,707 tonnes. RAS systems
are being operated on land and tested on pilot-scale
on floating structures in the Straits of Johor
SFA, 2020
Hong Kong
SRA (China)
Asia (South
China Sea)
7,428,887 19,596 / 7 4,133 124,299 Aquaculture includes marine fish culture, pond fish
culture and oyster culture. In 2019 production from
the aquaculture sector was 3,284 tonnes valued at
HKD 138 million. Currently, there are 26 marine fish
culture zones occupying a total sea area of 209 ha
with some 923 licensed operators. Majority of the
licensed farms are small, family-based and consisting
of one to two rafts. The estimated production in
2019 was about 889 tonnes valued at HKD 72
million which catered about 5% of local demand for
live marine fish. Other aquaculture production
includes pond fish culture in brackish and freshwater
and oyster culture, with 2,278 tonnes (HKD 52
million) and 117 tonnes (HKD 14 million) respectively
in 2019
AFCD, 2020
Salalah /Oman Middle East
(Arabian Sea)
374,582 3,385 / 51 451 553,445 Aquaculture in Oman began in 2003 with the
production of gilthead seabream representing 89
percent of the total. In 2004, aquaculture production
was valued at USD 2.5 million. Production of shrimp
started from 2007 with total production of 85 tonnes
and dominates the aquaculture production. There are
currently 21 integrated tilapia farms, one shrimp
Lund, 2019; The
Fish Site, 2020
(continued)
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 5
Table 1. Continued.
City (Country)
Region
(Water body)
Population
(hab.)
1
Port (10
3
TEUs) /
Rank
2
Aquaculture
production
(tonnes)
7
Fisheries
production
(tonnes)
7
Developing Aquaculture activities Reference
farm one marine cage farm in Oman. Oman’s
Ministry of Agriculture and Fisheries reported total
aquaculture production in 2019 at 1,054 tonnes
valuing OMR 2 million from sea bream and tilapia.
Cape Town area
(South Africa)
Africa (South
Atlantic Ocean)
3,740,026
3
882
5
/ - 7,868 570,545 Diverse marine species produced in South Africa with
mollusks (abalone, oyster and mussels) and trout as
dominant species produced. Region of Western Cape
has most farms accounting for 67% of South Africa
marine farms
DAFF, 2012; Britz & Venter, 2016
Valencia (Spain) Europe
(Mediterranean
Sea)
789,004 5,129 / 29 347,825 928,791 Valencia is a national hotbed of aquaculture production,
with output up to 9,278 metric tonnes of seafood
valued at EUR 38 million (USD 53 million) in 2011. In
its Fisheries Master Plan 2008-2013, the regional
Department of Agriculture, Fisheries, Food and Water
aimed to create new economic opportunities along
Valencia’s coast, providing employment, capitalizing
on local resources and encouraging investment.
Spanish aquaculture production reached a total
volume of 226,222 tonnes in 2013 for a total value
of EUR 429 million, mussel production representing
76.1% of total volume and 98 operational farms as
of 2014.
Towers, 2015;
European-
Commision,
2014b;
Dove, 2011
Rotterdam
(The Netherlands)
Europe (North Sea) 623,652 14,513 / 11 52,285 411,714 Three main production categories exist in the
Netherlands namely, the largest being that of blue
mussels as bottom cultures followed by oyster
production and then the land-based production of
fish, mostly eel and catfish. The Dutch aquaculture
sector is dominated by small companies with fewer
than 5 employees. As of 2011, there were 115
aquaculture farms (58 mussel production companies,
19 oyster production companies and 38 fish
production companies). The Dutch aquaculture sector
produced a total of 43,500 tonnes in 2011
amounting to EUR 64.4 million.
European-
Comission, 2014a
6 A. TROTTET ET AL.
Tampa Bay (United
States of America)
North America
(Gulf of Mexico)
3,091,399
4
57
6
/ - 468,185 4,756,997 Multiples aquaculture species including molluskan and
clams with a value of USD 71.6 million for 325 farms
in Florida in 2018.
FDACS, 2020
Vancouver
area (Canada)
North America
(Pacific Ocean)
675,218 3,397 / 50 191,323 839,224 Aquaculture in Canada is dominating by finfish
production with 149,418 tonnes produced in 2018
(equivalent of CAD 1.325 billion in 2018). Marine
salmon farming, which started in the early 1970s is
leading the market and most of the salmon are
produced in British Columbia with more than 87,000
tonnes for market value of CAD 772 million. Canada
is the 4
th
largest producer of salmon in the world.
Shellfish aquaculture is dominated by mussel and
oyster production, Prince Edwards Island as main
producer, with total production of 41,841 tonnes (¼
CAD 106 million) in 2018
Fisheries and
Oceans
Canada, 2020
Sydney (Australia) Oceania
(South Pacific)
4,321,535 2,648 / 72 96,799 186,576 Aquaculture in Australia represent AUD 1.42 billion
gross production value for 97.7 thousand tonnes
production in 2017-2018. Main species produced are
Salmonids (62% of Australia production,) followed by
Tunas (9%) and Oysters (7%). Barramundi and
Abalone are increasing in production representing
7% of production together. New South Wales hosts
shellfish production, which has increased from AUD
38 million in 2010-2011 to AUD 70.8 million in 2017-
2018. Production is dominated by one oyster,
Saccostrea glomerate (Sydney rock oyster) which
represent 51% of NSW production.
Farrell et al., 2013;
NSW EPA,
2020
1http://m.statisticstimes.com/demographics/countries-by-population-density.php.
2https://lloydslist.maritimeintelligence.informa.com/one-hundred-container-ports-2019.
3http://www.statssa.gov.za/?page_id=993&id=city-of-cape-town-municipality(2011).
4http://www.tampabay.com/blogs/baybuzz/2018/03/23/census-tampa-bay-saw-10th-biggest-metro-population-gain-in-2017.
5https://frontrunner-bucket.s3.amazonaws.com/2FC9C5A5-5056-907D-8DE3-152D117B6920.pdf.
6https://www.transnetnationalportsauthority.net/Commercial%20and%20Marketing/Pages/Port-Statistics.aspx.
7http://www.fao.org/fishery/statistics/global-production/query/en.
https://www.sfa.gov.sg/docs/default-source/tools-and-resources/yearly-statistics/local-production.pdf.
#
https://www.sfa.gov.sg/docs/default-source/food-farming/licensed-fishing-vessel.pdf.
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 7
economy based on knowledge and technology (Chou, 2006; Ludher &
Paramasilvam, 2018). Therefore, Singapore has become heavily reliant on
international food and water imports to meet over 90% of its daily require-
ments (Teng & Escaler, 2010). This dependence on imports and its sustain-
ability was challenged during the food crisis of 2008, when a stunted global
food supply chain and price fluctuations uncovered Singapore’s vulnerabil-
ity in maintaining food security (Teng & Escaler, 2010).
With a population projected to reach 6.9 million by 2030 and an average
of 10 million tourists per year, placing increasing pressure on the current
food sources, the government aims to increase food self-sufficiency, secure
good quality food at source at sustainable cost and regular supply (Sin,
2018; Teng & Escaler, 2010). Diversification of food imports from multiple
sources, contract farming with China and Malaysia for products consumed
in Singapore and increasing local productivity through innovative urban
farming were some of the approaches adopted to reduce dependency on a
single or few exporting countries (Teng & Escaler, 2010).
Seafood, especially fish, is a crucial component of the Singaporean diet
and many efforts have been directed toward achieving fish production to
supply 15% of local fish consumption (vs 5% in 2010), further limiting reli-
ance on international imports (Teng & Escaler, 2010). The Marine
Aquaculture Center (MAC) established in 2003 by Singapore Food Agency
(SFA) on St. John’s Island aims to increase Singapore’s annual fresh fish
production by developing large scale hatcheries and open cages to rear
fishes (Ludher & Paramasilvam, 2018; AVA, 2019).
Since the formation of the Singapore Food Agency (SFA) in 2019, there
was a greater focus on increasing local food production to meet 30% of the
nutritional needs by 2030, also known as “30 by 30”(SFA, 2020). Given
Singapore’s limited geographical spread and constant coastal developments,
achieving an increase in fish production requires better incentives for farm-
ers, higher public and private sector investments (local and international)
Figure 2. The urban areas described in this review are represented on a color-coded scheme
for the ratio of aquaculture to fisheries production in 2018 (except for production in Singapore
2019) and the recorded number of HAB occurrences represented by color coded dots till date.
8 A. TROTTET ET AL.
into research and development to adopt new technologies and maintenance
of optimal water quality (FAO, 2009, Teng & Escaler, 2010; Gin et al.,
2006; Schmoker et al., 2014). For example, the Aquaculture Innovation
Center (AIC) was established in June 2019 in collaboration with eight part-
ners including tertiary institutes (Temasek Polytechnic and other polytech-
nics, the National University of Singapore (NUS)), governmental agencies
(SFA), Agency for Science Technology and Research (ASTAR) and fish
Figure 3. Maps of each of the urban areas representing their aquaculture to fisheries produc-
tion ratio.
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 9
Table 2. Information on HABs events for each urban area with year, location, organisms involved, cause and characteristics with economic and/or environ-
mental losses. Mitigation and management measures are also included when available.
Year Location Organisms Causes and characteristics Economic / environmental loss Mitigation and management Reference
SINGAPORE
1987 Johor Straits Cochlodinium sp. Anthropogenic inputs,
warm weather
fish kills Gin et al., 2000
Unspecified Johor Straits Diatoms, Trichodesmium sp.,
Gymnodimnium-like species
Gin et al., 2000
1989 East Johor Straits Gymnodinium catenatum and
Chattonella sp.
caged fish kills Gin et al., 2006
Dec. 2009 East Johor Straits Karenia cf. australe 3.50 10 4 cells.L
-1
200,000 farmed fish mortalities Leong et al.,
2015; Trottet
et al., 2018
March 2010 East Johor Straits Chattonella subsalsa >500 cells.L
-1
Leong et al., 2015
Jan. 2011 Johor Straits Karenia mikimotoi >200 cells.L
-1
Leong et al., 2015
Dec. 2011 East Johor Straits Prorocentrum sp.; Chattonella subsalsa;
Heterosigma akashiwo
dominant species Prorocentrum sp.
>2,500 cells.L
-1
Leong et al., 2015
2012 Lim Chu Kang (West
Johor Straits)
Chattonella subsalsa >5,000 cells.L
-1
no associated fish kills Leong et al., 2015
June 2013 Lim Chu Kang fish farm -
North west of Singapore
Unidentified 90,000 kg farmed fish mortalities Leong et al.,
2015; Trottet
et al., 2018
Feb. 2014 East (Punggol Marina)
and West Johor Straits
Gymnodinium sp., Karlodinium
cf. veneficum,Takayama
xiamenensis
1.23 10 5 cells.L
-1
at Raffles
Marina (Tuas).
150,000 kg of farmed fish
mortalities from 53 fish farms
along the West Johor Straits
Leong et al., 2015
April 2014 East Johor Straits Karenia mikimotoi Patches of Karenia mikimotoi.>
5,000 cells.L
-1
. First time such
high cell densities were
recorded for this species
Trottet et al., 2018
Feb - March 2015 West Johor Straits 700,000 kg of farmed fish
mortalities ¼loss of SGD 1.3
million/farmer
Deployment of canvas bags to create a
closed containment unit and
emergency harvests saving market-
sized fish stocks
AVA., 2016; Trottet
et al., 2018
Dec 2016 East Johor Straits (shoreward
of Lower Seletar Reservoir
barrage)
Diatoms 1.52 10
4
± 652 cells.mL
1
Kok & Leong, 2019
Dec 2016 East Johor Straits (seaward
of Lower Seletar
Reservoir barrage)
Diatoms 3.18 10
4
±3.37 10
3
cells.mL
1
Kok & Leong, 2019
Jan 2016 East Johor Straits (shoreward
of Lower Seletar Reservoir
barrage)
Chattonella subsalsa (86.2%),
Heterosigma akashiwo (13.8%)
1.47 10
4
± 400 cells.mL
1
Kok & Leong, 2019
Jan 2016 East Johor Straits (seaward of
Lower Seletar
Reservoir barrage)
Chattonella subsalsa
Karenia mikimotoi, Ansanella sp.
142 ± 12 cells.mL
1
1.25 10
3
± 25 cells.mL
1
Kok & Leong, 2019
Feb 2016 East Johor Straits (shoreward of
Lower Seletar
Reservoir barrage)
Karenia mikimotoi (77.1%), Ansanella sp.
(22.7%) , Karlodinium sp.
3.94 10
3
± 153 cells.mL
1
Patches of Karenia mikimotoi.>
8000 cells.L
1
. Highest cell
Kok & Leong, 2019
10 A. TROTTET ET AL.
densities recorded for this
species in Singapore
Feb 2016 East Johor Straits (seaward of
Lower Seletar
Reservoir barrage)
Lauderia sp. , Skeletonema sp. 1.65 10
4
±1.71 10
3
cells.mL
1
Kok & Leong, 2019
Oct 2017 East Johor Straits (at jetty near the
causeway linking Singapore
and Malaysia)
Heterosigma akashiwo
Skeletonema sp., Chaetoceros sp
Major dinoflagellate species
:Gyrodinium spp, Protoperidinium spp.
Minor dinoflagellate species -
Scrippsiella sp. , Karlodinium sp
110 ± 4 cells.mL
1
2.58 104 ± 824 cells.mL
1
113 ± 14 cells.mL
1
Kok & Leong, 2019
Oct 2017 East Johor Straits (at mouth
opening into the
Singapore Straits)
Heterosigma akashiwo
Skeletonema sp., Chaetoceros sp
Major dinoflagellate species :
Gyrodinium spp, Protoperidinium spp.
Minor dinoflagellate species -
Scrippsiella sp. , Karlodinium sp
442 ± 21 cells.mL
1
4.39 103 ± 371 cells.mL
1
110 ± 8 cells.mL
1
Kok & Leong, 2019
Nov 2017 East Johor Straits (at jetty near the
causeway linking Singapore
and Malaysia)
Diatoms
Major dinoflagellate species :
Gyrodinium spp, Protoperidinium spp.
Minor dinoflagellate species -
Scrippsiella sp. , Karlodinium sp
2.99 10
3
± 304 cells.mL
1
124 ± 1 cells.mL
1
Kok & Leong, 2019
Nov 2017 East Johor Straits (at mouth
opening into the
Singapore Straits
Diatoms
Dinoflagellate
2.80 103 ± 28 cells.mL
1
55 ± 5 cells.mL
1
Kok & Leong, 2019
HONG KONG
1976 2001 Tolo Harbor Unidentified semi enclosed and poorly flushed
water body
Agriculture Fisheries and Conservation
Department (AFCD) acts as a
coordinator of Red Tide Reporting
Network, to investigate and warn
marine fish farmers of associated risks
and employs appropriate measures to
reduce loss. Since 1999, the
government has established the Red
Tide/HAB management framework and
various action plans such as: i)
Mariculture Action Plan by AFCD, ii)
Algal Biotoxin Action Plan by Food and
Environmental Hygiene Department
(FEHD) and Department of Health (DH)
and iii) Beach Action Plan by Leisure
and Cultural Services
Department (LCSD)
Lee et al., 2006;
AFCD, 2020
1988 Kat O, Long Harbor, Tolo Harbor,
Port Shelter and
southern waters
Unidentified major fish kills, fish culture zones
in Tolo harbor affected with
huge loss
Lee et al., 2006;
AFCD, 2020
late 1997 - early 1999 Phaeocystis globosa 1,500 tonnes of farmed fish killed
(50% of HK production
in 1998)
Tang et al., 2003;
AFCD, 2020
March 1998 - April 1998 Unidentified Tang et al., 2003;
AFCD, 2020
Nov. 1998 Gymnodenium cf catenatum Tang et al., 2003;
AFCD, 2020
Unspecified Karenia digitata 3,400 tonnes of cultured fish stock
(80%) - more than HKD
312 million
Wong et al., 2007;
AFCD, 2020
Unspecified Deep Bay in the west Unidentified nutrient inputs from heavily
contaminated Shenzen river
and Hong Kong
Lee et al., 2006;
AFCD, 2020
Unspecified Pearl river estuary Noctiluca scintillans, Skeletonema costatum,
Chattonella marina, Rhizosolenia alata f.
gracillima, Gonyaulax polygramma,
Pseudonitzschia pungens, Thalassiosira
subtilis, Scrippsiella trochoidea,
Prorocentrum sigmoides, and
Gymnodinium mikimotoi
high concentrations of inorganic
nitrogen, phosphate and
turbidity.
river discharge during dry
season(summer) as the river
plume is pushed seaward
Lee et al., 2006;
AFCD, 2020
(continued)
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 11
Table 2. Continued.
Year Location Organisms Causes and characteristics Economic / environmental loss Mitigation and management Reference
2015 Hong Kong waters Karenia mikimotoi Fish kill at Yim Tin Sai fish
culture zone
EPD, 2016
Jan-Feb 2016 Tolo and Long Harbors Karenia mikimotoi, K. papilionacea Estimated loss of about 220
tonnes of cultured fish (mainly
Sabah Grouper) at nine fish
culture zones
EPD, 2017
SALALAH / OMAN
Aug. 1976 Salalah (along the Salalagh coast
between Taqah and Raysut)
Unidentified first red tide in Oman mass mortality of fish - estimated
7,000 to 10,000 tons
Thangaraja et al., 2007;
Al-Azri et al., 2015;
Burt et al., 2016
Oct. 1976 Muscat Gonyaulax sp. and Noctiluca sp Thangaraja et al., 2007;
Al-Azri et al., 2015;
Burt et al., 2016
Feb. –April 1988 (2 times) Muscat,Sidab, Al-Bustan, Qantab Noctiluca scintillans Fish mortality (thousands of
pelagic fish)
Al-Azri et al., 2015
Sept. 1988 From Seeb to Qurm along 30km
coastal stretch, Al-Ghubrah
Ceratium fusus, C. macroceros and many
species of diatoms
Large blooms of diatoms caused
first discoloration of the water.
Low oxygen level was
recorded (2.64mg.L
-1
and
1.87 mg.L
-1
) at water depths of
2-3 meters and 8-10 meters
respectively.
First major fish kill in the Gulf of
Oman. 3 to 5 tons of dead fish
were strewn all along the Al-
Ghubra beach.
The regular monitoring of
phytoplankton blooms and red tide
phenomena in Omani waters were
initiated after this fish kill
Al-Azri et al., 2015
Feb. –Apr. 1989 (3 times) Qurum to Qantab Noctiluca scintillans Fish mortality Thangaraja et al., 2007
April 1989 Al-Ghubrah Rhizosolenia sp.
September 1989 Al-Ghubrah Pleurosigma sp., Ceratium spp. Mortality of marine organisms
March and May 1990 Al- Bustan, Mattrah (March) Sidab-
Al, Bustan (May)
Noctiluca scintillans, Ceratium furca, C.
macroceros,Prorocentrum micans,
Pyrophacus horologicum,Peridinium sp.
January 1990 Musandam Noctiluca scintillans
September 1990 Al-Ghubrah Rhizosolenia sp., Pleurosigma sp., Nitzchia sp.,
Coscinodiscus sp., Fragilaria sp.,
Triceratium sp., Chaetoceros sp.,
Ceratium spp.
Aug. –Sept. 1991 Muscat Coscinodiscus marginatus,Asteromptelus sp.,
Chaetoceros sp., Rhizosolenia sp.,
Ceratium spp.
March - April 1992 Al-Ghubrah and Al-Bustan Noctiluca scintillans
April 1992 Musandam (Dibba) Noctiluca scintillans
June 1992 Musandam (Khasab) Trichodesmium sp.
April 1993 Muscat, Sidab, Al-Bustan & Qantab Noctiluca scintillans Fish
September 1993 Mina Sultan Qaboos port Gonyaulax sp. Fish mortality (2-3 tonnes)
September 1993 Al-Bustan, Sidab Trichodesmium sp.
October 1993 Barka (Gulf of Oman) Dinophysis spp., Ceratium spp. Fish mortality
Aug. and Nov. 1993 Raysut Diatoms and Dinoflagellates Fish mortality
March, April and July 1994 Muscat, Qantab, Al-Bustan Noctiluca scintillans
12 A. TROTTET ET AL.
March 1994 Bimmah Noctiluca scintillans Thangaraja et al., 2007
September 1994 Bandar Khairan Noctiluca scintillans
August 1994 Mina Sultan Qaboos port/
Muttrah, Muscat
Gonyaulax sp. Fish mortality (50 kg)
January 1995 Kalbu Trichodesmium sp.
April 1995
Feb. –April 1996
Jan. and Feb. 1997
Muscat, Sidab, Al-Bustan Noctiluca scintillans
February 1997 Muscat –Sur (about 300.km.) Noctiluca scintillans
April 1997 Al-Bustan, Sidab Noctiluca scintillans
Aug. and Sept. 1999 Al-Bustan, Muscat, Al-Ghubrah Noctiluca scintillans (Green tide)
September 2000 Barka Coscinodiscus apiculatus,C. perforatus,C.
janischii,C. gigas and C. jonesianus
Depletion of dissolved oxygen. Second major fish kills recorded in
the Gulf of Oman
Aug. and Sept. 2000 Sidab and Bustan coast Gonyalaux sp./red tide
August 2001 Gonayalaux diegensis/ red tide bloom
November -December 2001 Arabian Sea Karenia selliformis, Prorocentrum micans,
P. minimum
Fish, turtles, dolphins and bird
mortalities. 27 tons of fish
were found floating near the
coast of Batinah, Sur and
South Oman
April 2004 Coast of Duqm 100 tonnes of sardines Piontkovski et al., 2012
October 2005 East of Masirah Island Noctiluca scintillans, Prorocentrum micans,
Trichodesmium erythraeum
Mortalities coincided with warmer
surface
temperatures, upwelling
Dead and weakened fish and
invertebrates observed on or
near the surface of the water
and along the tide line on the
shore. Large numbers of
swimming crabs (Portunidae)
observed on surface.
Busaidi et al., 2008
September 2006 Bay of Bandar Khayran Leptocylindrus minimus, Pseudo-nitzschia
delicatissima and pungens
abundances of 64 10 3 cells.L
-1
,
51 10 3 cells.L
-1
and 4710
3 cells.L
-1
respectively
Al-Azri et al., 2015
2006 and 2007 Bay of Bandar Khayran Dinophysis caudata and Gonyaulax spinifera higher abundances at 10 m Al-Azri et al., 2015
late SWM and early NEM
of 2008
Bay of Bandar Khayran Ceratium fusus more abundant at the surface Al-Azri et al., 2015
Oct. - Dec. 2008 from the North West of the Gulf
of Oman reaching the Bay of
Bandar Khayran and extended
to the south past Muscat and
several hundred km into the
Persian Gulf past the
Musandam peninsula
Cochlodinium polykrikoides Large fluctuations observed in
dinoflagellate abundances
ranging from 214 cells.L
-1
to
16 10
3
cells.L
-1
and up to
200 10
3
cells.L
-1
. Chlorophyll
levels were at a high of
78.0 lg/L. Bloom influenced by
an elevated nutrient load,
warmer than normal
temperatures and provoked
hypoxia. The bloom lasted for
10 months covering about
86,462 Km
2
across the
Arabian region.
200 tons of fish, including 70 tons
of caged fish, 70 tons of
shellfish, and 60 tons of wild
fish. Closure of desalination
plants due to clogging at the
intake resulting in serious
disruption of the potable
water supply, closure of
refineries, electric power
stations and tourist sites.
Schools closed in the Muscat
region due to intense odors
(methyl sulfide compounds)
and cancelation of beach
hotel bookings.
Richlen et al., 2010;
Berktay, 2011;
Al-Azri et al., 2012;
Al Shehhi et al., 2014;
Al-Azri et al., 2015;
Burt et al., 2016
(continued)
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 13
Table 2. Continued.
Year Location Organisms Causes and characteristics Economic / environmental loss Mitigation and management Reference
2006 2010 Bay of Bandar Khayran Prorocentrum minimum and
Scrippsiella trochoidea
abundances of these species were
significantly higher during
SWM (August–September).
Prorocentrum minimum
reached 1410
3
cells.L
-1
.
Scrippsiella trochoidea reached
13 10
3
cells.L
-1
.
Al-Azri et al., 2015
Fall and early winters 2006-
2011 (except 2008 and
2009 during C.
polykrikoides bloom)
Sea of Oman and Arabian Sea Noctiluca scintillans cell concentrations are higher
during NE and SW monsoons.
Moderate rain fall, wind
velocity and direction,
advection of water masses or
even the allelopathic
properties of C. polykrikoides
enhance N. scintillans blooms
Al-Azri et al., 2015
CAPE TOWN AREA
1994 Saint Helena Bay Alexandrium catenella and other
toxic species
Death of estimated 60 tonnes of
the West Coast rock lobster
Jasus lalandii (Milne Edwards),
and 1,500 tonnes of fish,
mainly the southern mullet,
Liza richardsonii (Smith)
Branch et al., 2013
January and May every year Along the west coast Commonly dominated by Dinophyceae, but
also Bacillariophyceae, Raphidophyceae,
Pelagophyceae, Haptophyceae,
Euglenophyceae
Vary yearly Branch et al., 2013
VALENCIA
1983 Balearic-Catalan Sea Alexandrium catenella Penna et al., 2005
1990 Mediterranean coast(Valencia) Gymnodinium catenatum 1.6 10 6 cells.L
-1
Vila et al., 2001
1994 Valencia harbor Alexandrium catenella abundance of 1.0 10 4 cells.L
-1
Penna et al., 2005
1998 and 1999 100km of the Catalan
coastline of Spain
Alexandrium catenella Penna et al., 2005
end of March-beginning of
April 2014
Prorocentrum cordata 10 3 cells.L
-1
ICES, 2017
2014 2016 harbor of Valencia Karlodinium sp 10 3 cells.L
-1
ICES, 2017
April and May 2016
2015 and 2016 harbor of Valencia Ostreopsis sp 3.9 10 3 cells.L
-1
and 2.910 3
cells.L
-1
ICES, 2017
June 2015 and May 2016 Valencia Pseudo-nitzschia sp. 3 10 5 cells.L
-1
ICES, 2017
May 2016 Dinophysis sacculus 1.410 3 cells.L
-1
ICES, 2017
Jan. and June 2016 Alicante Pseudo-nitzschia sp. ICES, 2017
Annual/Seasonal North Balearic front Unidentified late-winter/early-spring bloom
lasting for more than
three months
Garc
es & Camp, 2012
ROTTERDAM
2001 Originated in the Voordelta
offshore (between South
Phaeocystis globusa Enumeration of phytoplankton cells
from samples collected from
Van der Woerd
et al., 2006
14 A. TROTTET ET AL.
Holland and Zeeland) then
transported to shore
millions of cells.L
-1
and high
amounts of chlorophyll-a
provoke hypoxia
Economic damage to commercial
shellfish industry in the south
eastern part of the North Sea
monitoring, remote sensing
suggested as a monitoring measure.
2003 Voordelta, originated in the
Oosterschelde estuary which is
an area of intense mussel
cultivation
Phaeocystis globusa >10 million cells.L
-1
, chlorophyll-a
exceeding 40lg.L
-1
.
No mussel mortality. Unclear why
the bloom in 2001 caused
mass mussel mortality whereas
the bloom in 2003 did not,
although observed Phaeocystis
sp. concentrations did not
differ much.
The Dutch Ministry of Transport and
Public Works has maintained a
continuous monitoring in both fresh
and marine waters for suspended
matter, chlorophyll-aand
phytoplankton species composition.
Combination of remote sensing and
computer models to produce timely
and accurate information of HABs in
the coastal areas of the southern
North Sea.
Van der Woerd
et al., 2006
Annual basis South Bight of the North Sea Phaeocystis globosa summer and winter blooms Peperzak, 2003
Annual basis Dutch coastal zone Dinophysis acuminata,Prorocentrum
minimum,Pseudonitzschia multiseries,
Fibrocapsa japonica,Chattonella marina,
C. antiqua and Phaeocyctis globosa
high temperatures, salinity
stratification and irradiance in
late spring or summer
Peperzak, 2003
TAMPA BAY
2005-2006 South West of Florida The bloom persisted for 17 months Florida Fish and Wildlife (FWC)
Conservation Commission has
implemented HAB monitoring and fish
kills report accessible online
Maze et al., 2015;
fwc.com
2012-2013 South West of Florida Brevetoxin detected Death of hundreds of manatees
and other marine life
Maze et al.,
2015; fwc.com
Nov. 2015 - April 2016 Charlotte Harbor and Tampa
Bay region
Karenia brevis Charlotte Harbor region being
closed almost 40% of that
time period, while harvest in
Tampa Bay region was closed
almost 80% of the time. Loss
of USD 3.25 million dollars
Adams, 2017; fwc.com
Nov. 2017 - Jan. 2019 Tampa Bay region Karenia brevis The bloom happened two months
after Hurricane Irma: could be
related to release of water
from Florida’s Lake
Okeechobee to prevent
flooding, fertilizer-rich waters
flowed to the ocean and
helped fuel the current bloom
USD 90 million dollars in
tourism losses
Resnick, 2018; fwc.com
VANCOUVER AREA
late 1980s and 1990s Vancouver region Heterosigma akashiwo and Chaetoceros spp. physical damage or irritation of
gill tissues, reaction to ichthyotoxic
agents or hypoxia from
oxygen depletion
Salmon farms in BC and
Washington State lost in
excess of USD 35 million
Harmful Algae Monitoring Program
(HAMP) began in 1999, sampling
around Vancouver Island and in the BC
Central Coast. Weekly analysis for
harmful species identification and
count, consultation with salmon
aquaculture industry when HAB or fish
kills occur, training farm staff in
phytoplankton identification
Haigh and
Ensenkulova, 2014
1999 Vancouver region Cochlodinium sp. approximately CAD 2 million losses
2009 2012 British Columbia (BC) Heterosigma akashiwo,Chattonella cf.
marina,C.convolutus, and Chaetoceros
concavicornis
direct losses to BC salmon
aquaculture from HABs
exceeded CAD 16 million.
July-Aug 2011 Strait of Georgia (BC) Dinoflagellates (i.e. Dinophysis spp.,
Prorocentrum spp.)
62 clinical cases, closure of
harvest-zones
Taylor et al., 2013
(continued)
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 15
Table 2. Continued.
Year Location Organisms Causes and characteristics Economic / environmental loss Mitigation and management Reference
Diarrhetic Shellfish Poisoning (DSP)
due to consumption of
cooked mussels
Canadian Shellfish Sanitation Program
(CSSP) leaded by Canadian Food
Inspection Agency
2014 Marsh, Port Hardy Heterosigma akashiwo bloom 280,000 dead salmons Towers, 2015
2018 Vancouver region Heterosigma akashiwo bloom gills irritation 250,000 dead fish (1,000 tonnes)
in two salmon fish farms
estimated to CAD 4
million loss
Robinson, 2018
SYDNEY
Unspecified South Eastern Region Alexandrium spp. Monitoring programs are implemented
by each state (NSW Shellfish
Program includes Sydney)
Farrell et al., 2013;
Ajani et al.,2013
2010 South Eastern Region Alexandrium sp. Farrell et al., 2013;
Ajani et al.,2013
Unspecified coasts and estuaries in South
eastern Australia
Unidentified Mortalities of large numbers of
finfish, mollusks and
crustaceans
The Marine Biotoxin Management Plan
outlines ‘‘Phytoplankton Action
Limits’’ (PALs) whereby additional
shellfish flesh testing and/or harvest
zone closures are initiated based on
cell concentrations of potentially
harmful algae. The minimum PAL
for Alexandrium spp. is 200 cells.L
-1
Murray et al., 2015
2011 Jervis Bay, South eastern Australia Karlodinium veneficum fish kills Murray et al., 2015
2012 Coastal lagoon, Sydney Amphidinium cartarae Murray et al., 2015
16 A. TROTTET ET AL.
farms to work together aiming to increase the local seafood production
through high tech urban marine farming focusing on nutrition, disease
management and breeding of super fish (Begum, 2019). Other methods
that Singapore has adopted are to increase contract farming agreements for
seafood as well as increase the number of open water and land-based aqua-
culture farms (Teng & Escaler, 2010).
One of the most important factors that determines successful and large-
scale aquaculture practices rely on good water quality with minimal pollu-
tion and a good balance in nutrient levels. The rapid coastal developments
over the past 50 years such as port activities, land reclamation, oil refin-
eries, desalination and waste treatment plants, aquaculture and other indus-
tries have affected the water quality causing it to be eutrophic in the Straits
of Johor and oligo-to-mesotrophic in the Straits of Singapore (Ch
enard
et al., 2019; Gin et al., 2000,2006; Kok & Leong, 2019). Such anthropo-
genic activities have triggered HABs in Singapore causing massive fish kills
and tremendous economic losses as described in Table 2.
Singapore’sdependencyisinnotlimitedtofoodsolelybutalsoon
water supply. To date 60% of Singapore’s daily water requirements is met
with the water import contract with Malaysia, which expires in 2061
(Leidinger & Hustiak, 2019). To increase water self-sufficiency, on-going
developments of desalination plants is estimated to provide 30% of the
drinking water by 2060 (Leidinger & Hustiak, 2019). The treated effluents
from these plants are discharged into Singapore waters following regula-
tions where it is diluted and dispersed (Gin et al., 2006). These additional
nutrient loading can potentially exacerbate the issue of eutrophication
and of HABs.
The occurrences of HABs may also be caused by the introduction of inva-
sive species from ballast tank discharges from ships called to Singapore ports.
Ballast water may include dinoflagellate species such as Gymnodinium cate-
natum and Karlodinium sp. in the form of resting stages that had never
been previously described to be native to the region (Chan et al., 2006;Gin
et al., 2006; Trottet et al., 2018). Furthermore, there is evidence of the pres-
ence of the resting stages/cysts in the sediments of the Johor Straits which
can occasionally be resuspended resulting in HABs (Trottet et al., 2018). The
frequency and extent of sediment re-suspension has increased due to the
intense ship traffic and associated propeller wash in the region (Liao
et al., 2015).
Most of the HABs occurring along the Johor Straits have caused hypoxia
and massive kills of marine organisms during bloom decay as described in
Table 2 (Gin et al., 2006). Apart from the issues caused by HABs, a study
commissioned by SFA had shown that the farms in Johor Straits have
almost reached their carrying capacity (Tan, 2020). Therefore, SFA is
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 17
considering the development of more aquaculture zones in the Singapore
Straits to ramp up and meet Singapore’s food production target by 2030
(Tan, 2020).
Despite the maritime activity, Singapore Straits has the potential to sup-
port further aquaculture developments (Chou, 2006). Unlike the Johor
Straits, only one fish farm is operating at present in the Singapore Straits
(Tan, 2020). These waters are teeming with high biodiversity in marine life,
good hydrodynamic factors enabling good water exchange and flushing
(Chou, 2006). Although HAB species can be found in the Singapore Straits,
the strong mixing of these waters seems to inhibit the establishment of
HAB blooms (Chan et al., 2006; Gin et al., 2006; Tan, 2020). However, the
planned expansion of farming in the area requires additional understanding
of the ecosystem including the fluctuation in algal cell densities, the flush-
ing and/or potential presence of resting stages all of which are crucial for
proper site selection for aquaculture (Trottet et al., 2018).
Water quality parameters of Singapore waters are routinely monitored by
the National Environment Agency (NEA) using real time systems and field
monitoring to collect key physical, chemical and microbiological parame-
ters (NEA, 2020). Specific water quality monitoring of coastal fish farms is
conducted by SFA. This data can be accessed online by farmers and a
‘color-coded SMS’alert system provides timely warning to farmers on
plankton levels which can help them to activate timely mitigation strategies
(AVA, 2016). An Inter-Agency Bloom Working Group and Inter-Agency
Management Framework was established by AVA for monitoring, provision
of timely updates and management of HABs (AVA, 2016). However, lim-
ited time series records contributing to baseline plankton data are available
(Schmoker et al., 2014; Trottet et al., 2018). The lack of information on
phytoplankton species identity, many of which are yet to be properly iden-
tified and characterized, is particularly worrying in view of the upcoming
aquaculture developments planned by Singapore (Trottet et al., 2018).
To circumvent risks associated with fluctuating water quality affecting
the open-net cage farms, SFA encourages farms to adopt the use of tech-
nology such as closed containment systems/recirculating aquaculture sys-
tems (RAS). Such technologies have been proposed as sustainable
technologies by SFA which provide a controlled environment for growth,
enable automation of processes enabling better deployment of manpower
and mitigate the impacts of farming on the environment (SFA, 2020).
Currently, RAS is being operated by Apollo Aquaculture on floating struc-
tures in the Straits of Johor by Aquaculture Center of Excellence (ACE)
and Singapore Aquaculture Technologies (SAT) (Ludher & Paramasilvam,
2018; AVA, 2019). Farmers can apply for the Agriculture Productivity
18 A. TROTTET ET AL.
Fund (APF) administered by SFA to improve or adopt new technologies
which contribute to sustainable aquaculture (SFA, 2020).
Comparative case studies in aquaculture practices and associated issues of
HABs from around the world
Hong Kong - SAR China
The Hong Kong Special Administrative Region (HKSAR) has a sea area of
1,648 km for a coastline which is 1,197 km long. Excluding Hong Kong
Island and Lantau Island, there are 261 islands in the territory (EPD,
2019). Hong Kong is a highly developed territory and has become one of
the most significant commercial ports of the world (Table 1,Figures 2 and
3). Hong Kong is located at the south east corners of the Pearl River
Estuary (PRE), which for the last 30 years has received a very high load of
anthropogenic nutrients due to rapid industrial developments, agricultural
activities and urbanization (Lu & Gan, 2015).
In Hong Kong, seafood consumption has reached approximately 70 kg
per capita in 2017 which is four times the global average of 18.9 kg (FAO,
2020a). Even if local seafood production from aquaculture does not meet
the local demand, and therefore most products must be directly imported
from China, aquaculture does still exist in Hong Kong and is characterized
by a diverse production of fish in marine water (high value), ponds (main
contributor by volume), but also oyster production (Table 1). The marine
fish farming is mostly comprised of small size farms (294 m
2
) and is
located from Tolo Harbor on eastern side, to Lamma Island in the south to
Lantau Island in the west (AFCD, 2020).
Due to the high nutrient loads and organic wastewater discharges from
the PRE and local sewage discharges, the coastal waters in Hong Kong
experience frequent HAB events (Wong et al., 2009; Yin et al., 2000). The
most common species encountered during phytoplankton blooms in Hong
Kong waters is Noctiluca scintillans which accounts for 31% of reported
events between 1980 and 2015 (EPD, 2016). Algae bloom events have been
associated with seasonal variations and physical processes, with HABs being
observed more often during the winter- spring period when downwelling
allows phytoplankton biomass to increase (Xu et al., 2010). In summer,
rainfalls generate runoff events which reduce water residence times and
thus decrease phytoplankton concentration in more enclosed areas (i.e.
bays, harbors) (EPD, 2019; Xu et al., 2010). Geographically, data analyses
have shown that events occurred more frequently in the eastern and south-
ern waters of Hong Kong and these events reached peaks in 1988 with 88
incidents reported to reduce to 8-45 events per year (EPD, 2016). The
Environmental Protection Department (EPD) has implemented a marine
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 19
water quality monitoring program since 1986 to i) evaluate the state of
marine waters, ii) monitor long term change of water quality, iii) provide
proper scientific data for planning water pollution strategies (EPD, 2019).
This monthly monitoring includes traditional physico-chemical water qual-
ity analyses, sediment quality and phytoplankton sampling. In the late
1990s, sewage management strategies were implemented for sewage reduc-
tion by the government, which was successful in the case of Tolo Harbor
where a reduction of 90% in sewage loading has resulted in significant
decrease of inorganic nutrient loads directly reducing eutrophication (Xu
et al., 2010).
The EPD monitoring is associated with additional monitoring by
Agriculture Fisheries and Conservation Department (AFCD) which leads
HAB management framework and action plans (Table 1). Additional to
regular water quality monitoring, AFCD has put into place a specific real
time online water quality monitoring at 13 fish culture zones for early
detection of changes and issuance of alerts to mariculturists which is
accessible online
1
. Regular phytoplankton monitoring is also put into place
in all fish culture zones with increased monitoring frequency when harmful
species or high density of phytoplankton is observed to inform and alert
farmers if needed and weekly updates on algae bloom events made access-
ible online on AFCD website
2
.
Salalah (Oman)
Situated in the Middle East, the coast of Oman is a shallow continental
shelf, surrounded by the Straits of Hormuz in the North, Gulf of Oman in
the North-East and the western Arabian Sea in the South (Al Shehhi et al.,
2014)(Table 1,Figures 2 and 3). The western Arabian Sea connects to the
Gulf of Oman at the frontal zone of Ras Al Hadd and the Gulf borders the
coast of Iran and Pakistan in the north, (Al Shehhi et al., 2014; Harrison
et al., 2017). The water basins along the coastline of Oman are crucial ship-
ping and trade routes for exports of crude oil and others with high oil
tanker traffic (Al Shehhi et al., 2014). Oman experiences two monsoon
cycles namely the South-West (SW) summer monsoon from June to
September, contributing 70-90% of annual rainfall, and the North-East
(NE) winter monsoon from November to March (Al Shehhi et al., 2014).
Moreover, frequent sandstorms during the intermonsoon period from May
to July bring in dust deposition of iron (Al Shehhi et al., 2014).
The distribution of nutrients in the coastal waters of Oman are governed
mainly by seasonal monsoon dynamics especially the SW monsoon, when
1
http://202.74.40.143/afcdxyle/main_en.php
2
https://www.afcd.gov.hk/english/fisheries/hkredtide/update/redtide_cur_week.html
20 A. TROTTET ET AL.
dust deposition of iron from the sandstorms and upwelling, increase the
input of limiting nutrients and thereby favoring biological productivity (Al
Shehhi et al., 2014; Harrison et al., 2017; Piontkovski et al., 2012; Zhao
et al., 2015). This characteristic along with the shallow continental shelf
enabling cold water access for land-based aquaculture and its proximity to
bigger seafood markets (United Arab Emirates, India and South Africa)
make Oman an ideal place for aquaculture development (Lund, 2019).
Oman intends to develop its fisheries and aquaculture industry to be one
of the five main economic pillars through the Fisheries and Aquaculture
Vision 2040 (Vision 2040) targeting to produce 220,000 tons of fish per
year (USD 500-900 million) and creating 11,000 jobs (Lund, 2019).
Currently products from the 23 aquaculture farms in Oman as detailed in
Table 1 sustain the local seafood markets (Lund, 2019). According to
Vision 2040, The Oman Aquaculture Development Company (ODAC)
channels resources for foreign investments and expertise to secure growth
(Lund, 2019). Thus, the Ministry of Agriculture and Fisheries (MAF) have
streamlined seven zones spanning the entire coastline of Oman as potential
aquaculture sites for various species such as abalone, shellfish and seaweed
(Lund, 2019). The development of the aquaculture sector in Oman has
spurred international collaborations bringing together local and inter-
national expertise in various fields. For example, the MAF and the UK
Center for Environment Fisheries & Aquaculture Science (CEFAS) have
been working on guidelines for aquaculture health and disease management
(Lund, 2019).
Seasonal changes and increased anthropogenic inputs due to ongoing
coastal developments has led to increased nutrient loadings causing higher
frequency, intensity and expansion of HABs caused by diatoms and dino-
flagellates in the Gulf of Oman and the Arabian Sea in the last few decades
as described in Table 2 (Al Shehhi et al., 2014; Al-Azri et al., 2015).
Seasons play an important role in the distribution of nutrients, the NE
monsoon is known to cause more HABs than the SW monsoon due to its
strong winter convective mixing (i.e. Notiluca scintillans as in Table 2) (Al
Shehhi et al., 2014). The SW monsoons are known to cause dinoflagellate
and cyanobacteria specific HABs in the Arabian Sea due to strong winds
which cause the water to mix leading to high nutrient enrichments, strong
upwelling along the coastal margins in the south of Oman, higher sea tem-
peratures and river discharges (i.e. October 2005 in Table 2) (Al Shehhi
et al., 2014; Al-Azri et al., 2012; Burt et al., 2016; Busaidi et al., 2008).
Apart from transporting nutrients, currents in the Straits of Hormuz,
Gulf of Oman and Arabian Sea also cause the natural dispersion of HAB
species making the entire basin highly susceptible to blooms (Al Shehhi
et al., 2014). A good example of this dispersion was observed in 2008 when
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 21
the Cochlodinium polykrikoides bloom, firstly observed in the NW Gulf of
Oman in late October, extended its geographical impacts throughout the
entire Gulf of Oman and Arabian sea by early December aided by eddies
(Al Shehhi et al., 2014; Al-Azri et al., 2014; Zhao et al., 2015).
Huge amounts of fish-kills and closures of desalination plants were the
notable economic impacts reported in Oman due to HABs as detailed in
Table 2 (Al Shehhi et al., 2014). Desalination plants are extremely crucial
in the arid Arabian region as it is an important source of drinking water
accounting for 90% of potable water (Zhao et al., 2015). The presence of
HABs clogs the intake filters, cause bio-fouling of the sensitive reverse
osmosis membranes compromising the quality of desalinated water due to
its inability to remove toxins, eventually causing them to shut down for
expensive repairs resulting in a shortage of drinking water and electricity
shutdowns as seen during the Cochlodinium sp. bloom in March 2009 (Al
Shehhi et al., 2014; Al-Azri et al., 2014,2015; Richlen et al., 2010; Zhao
et al., 2015).
The Arabian Seas with high shipping traffic are also affected by oil spills,
bio-invasion through ballast water, ship hulks and other forms of pollution
(Al Shehhi et al., 2014; Al-Azri et al., 2015). Thus, some HAB species
detected in the Gulf of Oman and Arabian Sea manifest a shift in their
regular geographic distribution suggesting their global expansion such as
the Cochlodinium polykrikoides bloom occurring for the very first time in
Oman in 2008 (Al-Azri et al., 2015; Zhao et al., 2015).
There is a lack of baseline plankton composition and abundance data in
the coastal waters of Oman (Al-Azri et al., 2015; Thangaraja et al., 2007).
Satellite image monitoring such as MERIS fluorescence data accurately
detected the Cochlodinium polykirkoides bloom in 2008, providing species-
specific signatures and enabling it to be distinguished from other species in
the region despite environmental disturbances (Zhao et al., 2015).
Cape Town –South Africa
Located on the southwestern side of South Africa, Cape Town is the second
most populated city in South Africa after Johannesburg, having more than
60% of the population of the Western Cape province (Table 1,Figures 2
and 3). Cape Town shore which is part of Table Bay is one of the richest
fisheries zone in the world as it is influenced by the Benguela current, a
cold body of water moving up the western coastline of southern Africa
bringing accumulated nutrients from the sea floor, which when coupled
with sunlight provides massive phytoplankton blooms sustaining fisheries
(Branch et al., 2013; Pitcher et al., 1998; Pitcher & Greville, 2006).
The aquaculture sector in South Africa is largely dominated by maricul-
ture and is expected to increase continuously within the next 10 years
22 A. TROTTET ET AL.
(Britz & Venter, 2016). This is part of South Africa’s National
Development Plan and Vision 2030, as a sector with high growth potential
to alleviating poverty, unemployment and inequality through enhanced
food security (Hayes, 2013). For aquaculture, the governmental actions
included both regulations and financial support since 2013. The
Government has adopted a unified National Aquaculture Policy Framework
and launched an Aquaculture Development Enhancement Programme pro-
viding 45 million USD to support farmers to buy equipment and increase
job creation (Hayes, 2013, GCIS, 2013). A first edition of the legal guide
for the aquaculture sector in South Africa was instituted by the
Department of Agriculture, Forestry and Fisheries (DAFF). Although the
marine sub-sector operates less than 50 farms, compared to almost 200
freshwater operations, it accounts for approximately two-thirds of produc-
tion volume and more than 80% of value, mainly due to the contribution
of the well-established, high-value abalone sub-sector (Britz & Venter,
2016) with productions expected to further increase by 61.8% from 2018 to
2030 (FAO, 2020a).
Algal blooms commonly occur along the South African west coast and
have been recorded since March 1994, when a dense bloom developed due
to upwelling and causing fish kills at times (Branch et al., 2013,Table 2).
Although no proper HAB monitoring strategies have been implemented in
the country, the use of satellite imagery has enabled the detection of HAB
events which persisted from March to June 2017 off the western South
African’coast in the southern Benguela current (Ever-King et al., 2020).
Additionally, the South National Biodiversity Institute (SANBI) has estab-
lished the first comprehensive National Biosystematics Research Strategy
that deliberately emphasizes the research component of taxonomy for mul-
tiple organisms including algae and archaea between 2013 and 2018, pro-
moting taxonomic research throughout South Africa (Victor et al., 2013).
Valencia -Spain
Valencia, the third largest city in Spain, borders the North Western (NW)
Mediterranean Sea which is a semi-enclosed body of water connecting to
the Atlantic Ocean through the Gibraltar Straits (Table 1,Figures 2 and 3)
(Dove, 2011; Penna et al., 2005). The increasing number of ports, harbors,
housing, paved roads, tourism and recreational activities along the coast of
Valencia have led to eutrophication in the western Mediterranean basin
and specifically in the Gulf of Valencia, transforming it from one of the
most oligotrophic basins’in the world to one becoming increasingly
eutrophic (Gadea et al., 2013; Garc
es & Camp, 2012).
This region has recently secured significant growth in the aquaculture
sector, farming a variety of seafood species, enabling more investments and
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 23
providing opportunities for employment (Table 1) (Dove, 2011). The qual-
ity of Valencia’s waters allows for cultivation of diverse species (Dove,
2011; Ministry of Environmental Rural and Marine Affairs, 2011). The
quality of the production and the growth of the sector is considered excep-
tional compared to other Spanish cities and is expected to supply the local
and international markets by reducing dependency on imported seafood
from France (Dove, 2011; Ministry of Environmental Rural and Marine
Affairs, 2011; Towers, 2015). This growth has been supported by a large
range of public and private institutions. The Funds for the Regulation and
Market Organization of Fishery and Aquaculture Products (FROM), the
National Food and Agriculture Research and technology Institute (INIA)
and the Spanish Aquaculture Observatory (OESA) works directly with the
Ministry of Agriculture, Fisheries and Food for the promotion of aquacul-
ture products within local markets and conducts research related to path-
ology and the development of the aquaculture sector in Spain (FAO,
2017a). Such impressive growth in the aquaculture industry in Valencia
and other Spanish cities has made Spain one of the top Member State of
the European Union in terms of aquaculture production (Towers, 2015).
However, increasing frequency and intensity of HABs in the past 50years
have been recorded in the North Western (NW) Mediterranean basin,
including the Gulf of Valencia (Table 2;Pennaetal.,2005; Gadea et al.,
2013). Records of HAB events have since expanded along the Spanish coast-
lines and include paralytic shellfish poisoning (PSP) dinoflagellate
Alexandrium catenella (Garc
es & Camp, 2012;Pennaetal.,2005). Ballast
water exchange without use of ballast water treatment systems has been con-
sidered the vector of A. catenella spread in the Mediterranean Basin from its
natural habitat in the Western Pacific Ocean (Penna et al., 2005). Although
the shipping industry is crucial for trade including that of aquaculture prod-
ucts, it “poses biosecurity risks for the aquaculture”industry through the
introduction of invasive species which could cause potential HAB outbreaks,
impairing food security measures and human health (Drillet et al., 2018).
In addition to anthropogenic influences, seasonal dinoflagellate spring
blooms in the neighboring waters challenge the operations of many aqua-
culture farms warranting stricter monitoring (Gadea et al., 2013; Garc
es &
Camp, 2012; ICES, 2017). The National Advisory Board for Marine
Aquaculture (JACUMAR), the official institute involved in the mitigation
of HABs, has ordered a number of farm closures during HAB outbreaks
causing massive economic losses (FAO, 2017a; ICES, 2017).
Rotterdam –The Netherlands
The Netherlands is a densely populated country in western Europe and
despite its lack of natural resources, it is one of the largest exporters of
24 A. TROTTET ET AL.
agricultural products in the world (Viviano, 2017). As a result, the port of
Rotterdam has grown to become the largest port in Western Europe (Table
1,Figures 2 and 3) (Port of Rotterdam, 2019). Rotterdam is in proximity to
the Province of Zeeland located in the southern Dutch coastal zone which
is bordered by the southern North Sea (Van der Woerd et al., 2006). The
southern North Sea is maintained in a eutrophic state by river discharges
from the Nieuwe Waterweg of Rotterdam harbor, the Rhine, Meuse, other
small rivers and fish farms (Van der Woerd et al., 2006).
Although the aquaculture industry does not contribute significantly to
the Dutch economy, the shellfish industry is economically more significant
than finfish, with almost 60-70% of production being exported (FAO,
2017b). The aquaculture industry is expected to grow given the increasing
demand for fish products and increasing awareness on the benefits of fish
consumption both locally and internationally as well as generating more
employment and income (FAO, 2017b).
Shellfish cultivation is mainly practiced as bottom cultures in the estuaries
in the Southwest Province of Zeeland and in the shallow Wadden Sea bor-
dering the northern part of The Netherlands, representing an intense loading
of nutrients into the southern North Sea and impacting water quality (FAO,
2017b). In the past century, intense anthropogenic activities in the region
have created eutrophication issues in turn increasing the frequency and
intensity of high biomass phytoplankton blooms as well as toxin producing
HABs in spring and in summer as detailed in Table 2 (Peperzak, 2003;Van
der Woerd et al., 2006). Annual spring blooms, that develop offshore and
move near shore to sites of shellfish cultivation, are known to cause massive
economic loss to the shellfish industry (Van der Woerd et al., 2006).
Monitoring systems have been implemented by the Dutch Ministry of
Transport and Public Works and includes measurements of chemical and
biological parameters in marine and freshwater systems since 1970 (Van
der Woerd et al., 2006). The Netherlands have also implemented an early
warning system that uses remote-sensing satellite imagery (MERIS -
MEdium Resolution Imaging Spectrometer) to detect elevated chlorophyll-a
levels as a proxy for high biomass HABs. This early implementation was
proven to be successful in detecting offshore high biomass blooms (FAO,
2017b; Van der Woerd et al., 2006).
The Dutch aquaculture industry has evaluated the applicability of heated
RAS and vertical farming to produce more tropical species but this was seen
as an economical challenge due to its increased investment and operating
costs; therefore funds were allocated to support alternative production strat-
egies (FAO, 2017b). A national and provincial government funded initiative
to test out alternative breeding grounds such as outdoor basins and ponds to
the costly RAS commenced in 2007 to support farmers (FAO, 2009).
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 25
Tampa - USA
Tampa Bay, which consists of seven major water bodies, is Florida’s largest
open water estuary on the Gulf of Mexico coast extending over 1,000 km
2
characterized by subtropical climate providing heavy rainfall between June
and September (Table 1,Figures 2 and 3) (Sherwood et al., 2016; Wang
et al., 1999). For the past century the coast of Tampa Bay has undergone
drastic modifications associated with urbanization and, to a lower extent,
agriculture and phosphate mining that have affected its hydrology and
water quality (Sherwood et al., 2016). Port development and shipping activ-
ities have also been established since the 1880s and today Tampa Bay ranks
among the U.S.’s most productive ports (Sherwood et al., 2016;Table 1).
Although aquaculture is a relatively modest sector in the USA in terms of
production, the nation supplies a variety of advanced technologies, feed,
equipment and investment capital to other producers around the world
(NOAA Fisheries, 2020).AquacultureproductioninTampaBayisdomi-
nated economically by both oysters and clams, representing 80% of the pro-
duction values in 2017, followed by salmon, mussels and shrimps (National
Marine Fisheries Service, 2020). Florida, by its subtropical climate, extensive
marine and freshwater resources, cargo shipping and extensive coastline, has
also developed a uniquely diverse aquaculture sector (alligators, aquatic
plants, fish, bivalves) and was ranked 9
th
for total overall aquaculture values
in the USA in 2018 with USD 71.6 million (FDACS., 2020).
HABs have been occurring for decades and have caused considerable
damage to the environment and local economies. This poses a threat to
public health in Tampa Bay, with the last recorded event lasting more than
a year during a bloom of Karenia brevis. HAB events have been associated
with increased eutrophication due to the increasing population in Tampa
Bay from approximately 125,000 people in the 1950s to almost 4 million in
the late 2010s within the metropolitan community (Walsh et al., 2011). An
increase of chlorophyll-afrom 7 mg.L
1
in 1953 to 45 mg.L
1
in 1969 due
to releases of untreated sewage waters, rich in nitrogen and phosphorus
which enhanced biological productivity to such an extent that large blooms
of cyanobacteria Schizothrix calcicola were observed (Walsh et al., 2011).
With the implementation of wastewater treatment systems in 1979 to con-
trol severe eutrophication problems, inputs of nitrogen and phosphorus
decreased significantly, but blooms of dinoflagellates persisted presumably
due to accumulation of nutrients in sediments and presence of benthic
cysts of Alexandrium monilatum (Chen et al., 2010; Walsh et al., 2011).
Additional species of dinoflagellates were observed during such events,
such as Alexandrium spp, Pyrodinium bahamense or Karenia brevis, causing
multiple fish kills during the last decade. (ICES, 2017; Table 2, Maze et al.,
2015). To monitor such events, the Florida Fish and Wildlife Conservation
26 A. TROTTET ET AL.
Commission (FWC) has implemented a monthly HAB monitoring and fish
kills report which are accessible online (Chen et al., 2010). Recently, a
proposition to create Centers of Excellence on HABs have been introduced
by members of the US House to bolster the existing work on HABs, for-
malizing partnership between local, state and federal stakeholders to
develop ways to prevent, respond to and mitigate HABs (Derby, 2020).
An executive order was taken on May 7th, 2020 in the USA to promote
seafood competitiveness and economic growth by promoting Aquaculture
Opportunity Zones in federal waters to increase local aquaculture produc-
tion as 85% for fish and seafood are imported (NOAA Fisheries, 2020;
Smith, 2020).
Vancouver - Canada
Located on the west coast of Canada, Vancouver lies along the Strait of
Georgia which is the most densely populated region of British Columbia
(BC) with 75% of the total population of the region (Krepakevich &
Pospelova, 2010)(Table 1,Figures 2 and 3). The principal link between the
Pacific Ocean and inner Strait of Georgia is the Juan de Fuca Strait, which
is fed by deep, nutrient-rich flow enhanced by offshore upwelling and river
runoffs from the mainland (Krepakevich & Pospelova, 2010). The Strait of
Georgia experiences intense shipping traffic because it is the most used
marine channel in BC. Additionally urban developments with industrial
and commercial activities has contributed significantly to marine environ-
mental degradation (Radi et al., 2007). Inputs from rivers, sewage, ground-
water discharges are high and are associated with high nutrient
concentrations enhancing chlorophyll levels to as high as 20 mg.L
1
in
some areas (Radi et al., 2007).
As observed in other countries, seafood demands have increased in
Canada and seafood farming occurs in all provinces and territories with
about 56 species of organisms and plants commercially cultivated in mar-
ine, freshwater ecosystems, land-based ponds and tanks facilities. Farming,
fish processing activities represent significant economic benefits by generat-
ing CAD 2.2 billion in GDP and more than 26,000 jobs in 2017 (Canadian
Aquaculture Industry Alliance, 2018). As presented in Table 1, BC leads
the market by being the major producer in salmon through open cage
farming around Vancouver Island in the Pacific Ocean and the Strait of
Georgia (Haigh & Ensenkulova, 2014).
Since salmon farming industry began, HABs issues appeared and have
been identified as the largest cause of mortality of farmed salmon in BC in
early 2010s, costing millions of dollars (Table 2; Haigh & Ensenkulova,
2014). These events have been associated with diverse phytoplankton spe-
cies, such as the raphidophyte Heterosigma akashiwo, which was regularly
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 27
observed in salmon fish kills for the past 25 years (Table 2). Other species
observed belongs to diatoms and dinoflagellates (Table 2), the latter being
associated with a Diarrhetic Shellfish Poisoning (DSP) event due to con-
sumption of mussels in 2011 (Taylor et al., 2013). Associated with these
different events of fish kills and DSP, two specific monitoring regimes have
been implemented in BC. Following the different fish kill events from the
1990s, the monitoring program (HAMP) was implemented in collaboration
with fish farmers in BC (Table 2; Haigh & Ensenkulova, 2014). This pro-
gram was initiated under the egis of Fisheries and Oceans Canada (DFO)
in 1999 and run independently since 2004. HAMP has three mandates: i)
regular monitoring of selected sites near or at salmon farms with collection
of phytoplankton and environmental data; ii) real-time monitoring of fish-
killing blooms, and identification of causative species in support of salmon
aquaculture companies; and iii) education of farm personnel on sampling
and identification of marine phytoplankton, especially those species that have
been harmful to local fish (Environment and Climate Change Canada, 2019).
Regarding shellfish poisoning, the Canadian Shellfish Sanitation Program
(CSSP) was established to ensure that shellfish harvested in Canada are safe
for consumption and is a key component of the Government’s commitment
to protecting the health and safety of Canadians. Three federal government
agencies work together to deliver this program: i) the Environment and
Climate Change Canada analyzes water quality in shellfish harvesting areas
and identifies waters that do not meet sanitary standards, ii) the Canadian
Food Inspection Agency monitors for biotoxins in shellfish in harvesting
areas and is responsible for issuing licenses and inspecting shellfish that is
processed for interprovincial trade or export, and iii) the Fisheries and
Oceans Canada patrols and closes harvest areas, and bans the harvesting of
shellfish whenever bacteria or toxin levels exceed safety standards. Stringent
food safety guidelines for bacteria, biotoxins and other contaminants are set
by Health Canada (Environment and Climate Change Canada, 2019). Since
2015, a Citizen Science Oceanography Program funded by the Pacific
Salmon Foundation supported the Ocean and Networks Canada and DFO
has been implemented to monitor 80 defined locations simultaneously allow-
ing full coverage of the Strait of Georgia every year (Esenkulova & Pearsall,
2019). The monitoring includes phytoplankton analyses, enabling a better
understanding of the seasonal and spatial variations along the Strait of
Georgia (Esenkulova & Pearsall, 2019)
Sydney - Australia
Located on the east coast of Australia, Sydney is the New South Wales
(NSW) capital and with its surroundings regroup 65% of the population of
NSW (SMCMA, 2011). Botany Bay (to the south of Sydney) is influenced
28 A. TROTTET ET AL.
by intense anthropic inputs from its catchment area draining through
Georges and Cook Rivers (SMCMA, 2011)(Table 1,Figures and 3). The
main pollutions are related to industrial and urban development, character-
ized by chemical pollutions (metals) and storm waters (nutrients) (Spooner
et al., 2003; SMCMA, 2011). The Bay is also influenced from its contact to
the Pacific Ocean. Botany Bay hosts the busiest airport of Australia on its
northwestern side and a large container terminal on the east. The southern
shore of the bay, despite its relative isolation, is dominated by an unusual
mixture of pristine national parks and heavy industrial activities including
a desalination plant, a fuel terminal, a sewage treatment plant and historical
sand mining facilities (SMCMA, 2011). By its proximity to Sydney, Botany
Bay has been a logical site for industrial development for decades, associ-
ated with residential development in the neighborhood. Port Botany, the
second busiest port in Australia has recently undergone a major expansion
of its shipping container operations and some major industries (NSW
EPA, 2020).
Seafood demand in Australia has increased considerably over the last
three decades and current consumer demand for seafood exceeds the sup-
ply from domestic production and is predicted to continue to grow
(ABARES, 2020). Aquaculture production occurs from the tropical north to
the temperate south which allows the production of multiple species. In
NSW, Sydney rock oysters represent the main production (Table 1), grown
with other species along the 2,000 km of coastline and estuaries such as
Botany Bay/Georges River area (Farrell et al., 2018).
HABs have been encountered for decades in Australia and have been
associated with some fish kills in the area of Botany Bay/Georges River
HABs (Table 2; Farrell et al., 2013; Murray et al., 2015). NSW agencies
reported approximately 20 events of fish kills annually over the past
40 years, affecting shellfish, finfish and crustaceans (Murray et al., 2015).
Out of the 20 HAB species identified in Botany Bay/Georges River near
oyster growing areas, most of them are dinoflagellates (Ajani et al., 2013)
such as Amphidinium caterae, Dinophysis caudata, or Karlodinium venefi-
cum and Alexandrium spp. (Murray et al., 2015, Farrell et al., 2018).
Alexandrium sp. resting stages have been identified in Georges River (Tian
et al., 2018). Monitoring programs have been implemented by each of the
Australian states and in NSW, the Shellfish Program and the Marine
Biotoxin Management Plan have been implemented to provide
“phytoplankton action limits”(PAL) to determine potential harvest zone
closures depending on cell concentrations levels of harmful species (e.g.
PAL of Alexandrium spp. is 200 cells.L
1
and 500 cells.L-1 for Dinophysis
spp.) (Ajani et al., 2013; Farrell et al., 2013; NSW FA, 2017). A Water
Quality Improvement Plan has been developed for Botany Bay and its
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 29
catchment to reduce pollution loads by 2030 for total nitrogen, total phos-
phorus and total suspended solids (SMCMA, 2011) as nutrient loads have a
direct impact on chlorophyll-aconcentrations by encouraging productivity.
Comparing and contrasting the strategies adopted by different countries to
develop the aquaculture sector and mitigate the impacts of HABs
With increasing population, the development of aquaculture has proven to
be an extremely good option to ensure food security (uninterrupted supply
and good quality of food).
Different urban areas face different challenges in sustainably increasing
their aquaculture production with respect to the following:
Geography –space allocation
Economy –resources for training, collaborations and building infrastructure
Ecology –HAB occurrences and mitigation
We recognize that the criteria mentioned above are limited to the data
available summarized in the previous sections.
This section evaluates the various methods adopted by the urban areas of
the aforementioned countries to develop their respective aquaculture sector,
extrapolate the applicability of some of these strategies to other countries,
their associated constraints and the potential solutions that can circumvent
these production issues.
Section 1: Improving aquaculture production with modern farming
and education
Rapid extension of aquaculture in different cities/countries undergoing
increased urbanization, brings about space constraints and increased public
concerns on risks to the degradation of aquatic ecosystem (Galland &
McDaniels, 2008; Hamouda et al., 2005). New ways for sustainable aquacul-
ture such as RAS, allows control of key parameters such as water quality,
effluent and solid waste release, protection against predators and harmful
events such as HABs (Losordo et al., 2009). Therefore, urban areas with
space constraints and intense nutrient loadings such as Singapore, have
encouraged some farms to adopt technologies such as the RAS. In combin-
ation with other coastal farms, Singapore’s local production levels for fish
has reached almost 10% of the annual total consumption of food fish in
2019 (Moore & Guerrero, 2020). Such methods could be potentially applied
in other countries facing similar space constraint issues such as Hong Kong.
In comparison, aquaculture farms in countries like Oman, are not con-
strained by space but constantly challenged by seasonal blooms, that could
30 A. TROTTET ET AL.
be mitigated by the introduction of RAS, using cold waters from their shal-
low continental shelves (Lund, 2019). Similarly, Valencia does not face spa-
tial constraints, but the waters of the Gulf of Valencia are constantly
plagued by seasonal blooms forcing farm shutdowns. Here too, RAS sys-
tems could serve as a great alternative to supplement production. However,
such farming infrastructure is expensive to build, requires trained farmers
and might not be economically viable depending on the market price of the
type of organisms produced (Losordo et al., 2009). For example, in the
Netherlands, the high operating cost has been identified as a limitation of
RAS due to the cold waters of the south North Sea (FAO, 2017b).
Other recent technological developments have enabled offshore aquaculture
practices further away from the coastlines, where space is not an issue.
Following Drumm’s definition (2010), “offshore aquaculture may be defined as
taking place in the open sea with significant exposure to wind and wave
action, and where there is a requirement for equipment and servicing vessels
to survive and operate in severe sea conditions from time to time. The issue of
distance from the coast or from a safe harbor or shore base is often but not
always a factor”. Such production reduces potential environmental impacts by
allowing farm discharges to be diluted in larger open areas, creating a natural
“dilution”of aquaculture effluents, thus limiting the environmental impact of
the discharge as mentioned by Welch et al. (2019). This development is not
universally approved and concerns have been pronounced regarding proper
environmental data assessment for this new farming technique to ensure
proper implementation (Simke, 2020). Some long-term data on offshore aqua-
culture have been published and the results suggest little or no impact on
water quality and sediment enrichment (Welch et al., 2019). Oman, while
moving toward its 2040 plan, is currently building offshore farms as an effect-
ive strategy to minimize nutrient loading from aquaculture activities
(Lund, 2019).
Modernization of aquaculture needs skilled workers, highlighting the
need for proper training such as the official inclusion of aquaculture
courses into academic programs which would help to nurture a workforce
dedicated toward the sustainable and profitable expansion of the sector
(FAO, 2017a). Moreover, Southeast Asian Fisheries Development Center/
Aquaculture Department (SEAFDEC/AQD) encourages the sustainable
development and the responsible stewardship of aquaculture by promoting
science-based aquaculture technologies, developing and strengthening
capacities through training in the Southeast Asian region. Thus, providing
both knowledge-based and technical skills to farmers setting up new aqua-
culture businesses (FAO, 2017a). In addition, public awareness on the
interdependency of HABs and aquaculture through regular campaigns and
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 31
public involvement in visual HAB detection is on the rise as witnessed in
Canada, US and Europe (Lauro et al., 2014, Esenkulova & Pearsall, 2019).
Section 2: Monitoring and mitigation strategies
Wherever open cage fish farms are implemented, proper governmental reg-
ulations need to be enforced for site selection and environmental impact
assessment (EIA) to determine the optimal carrying capacity of the farms
and the associated risks. The administration of EIA has been implemented
in different countries such as Singapore, United States, or Europe, with cri-
teria for risk evaluation varying from one country to another. Transition
from familial businesses to global companies through investments and
acquisitions to adopt high tech farming strategies can improve and increase
productions (Basu, 2019).
As observed in other intensive large-scale production systems, diseases
by pathogens (recurring or new) (e.g. shrimp ‘glass postlarvae’in China)
and effective control of infectious diseases are also a very important con-
cern in aquaculture (Harkel, 2020). The nature of the sector’s production
systems, ongoing intensification, reliance on international trade, importance
for livelihoods and food security in resource-limited countries, make it
prone and extremely sensitive to the impact and spread of diseases. As per
traditional water quality monitoring, understanding the life cycle of patho-
gens, genetic screening coupled to modeling could be key in effective man-
agement of the sector.
As observed in Oman, Hong Kong, Cape Town, Rotterdam and
Valencia, HAB events can display seasonal patterns requiring altered course
of farm operations. Such outbreaks further aggravate the economic con-
cerns as they can cause shutdowns of desalination plants as seen in Oman
and further brings about water shortages in the region.
Farming practices are also under increasing pressure by emerging threats
such as the input of plastics in the marine environment. In particular,
microplastic particles can be ingested by marine organisms, resulting in the
bioaccumulation of toxic substances in the food chain and ultimately affect-
ing human health (Lusher et al., 2017). This will impact some aquaculture
sectors more than others since the likelihood of humans ingesting micro-
plastic particles while consuming seafood is small for many of the larger
fish species (where the gastrointestinal tract of the fish is removed), but
higher for bivalves and several species of small fishes which are consumed
whole. Furthermore, microplastic particles have been shown to act as a hot-
spot for the dispersal of HABs (Mas
o et al., 2003) and the accumulation of
human pathogens (Bowley et al., 2021), which could directly affect both
aquaculture and human health.
32 A. TROTTET ET AL.
Therefore, as urbanization processes continues and aquaculture opera-
tions need to be expanded to ensure adequate food for the growing popula-
tion, proper regular monitoring of water quality regime should be enforced
including physical, chemical and biological parameters as detailed in the
examples of this review. When possible the use of satellite imagery coupled
with monitoring, can become an efficient warning system for high biomass
HABs especially those occurring offshore as seen in Rotterdam during the
2001 bloom (Van der Woerd et al., 2006). This information when incorpo-
rated into hydrodynamic and ecological models could be pivotal in the
forecasting of water quality and HABs. Additionally, the use of inexpensive,
rapid and portable third generation sequencing devices (e.g. Oxford
Nanopore MinION), incorporated into regular monitoring can enable the
precise characterization of microalgal species (George et al., in-press). Such
monitoring and predictive modeling results should be made accessible to
professionals, decision makers, potentially to the public and when coupled
with proper mitigation measures, developed according to Governmental
policies, ensure the sustainability of aquaculture operations and other
industrial activities. A good example where information of this nature is
made publicly available online since early 2000 is in Hong Kong based on
their regular and long-term monitoring procedures.
Furthermore, engaging citizen scientists and other partners to monitor
the onset of harmful algal blooms and help to rapidly characterize their
identity may also become an economical way to address HABs holistically
(Lauro et al., 2014, Esenkulova & Pearsall, 2019, Murray Darling Citizen
Scientists
3
).
Conclusion
As of today, the ongoing COVID-19 pandemic has affected the world glo-
bally and to reduce the spreading of the virus many countries have insti-
tuted stricter regulations and border closures. The implemented lockdowns
have resulted in logistical difficulties in seafood trade, particularly in rela-
tion to transportation and border restrictions (FAO, 2020b). The shrimp
and salmon industries, in particular, have suffered from increased air
freight costs and cancelation of flights (FAO, 2020b). Some shortages of
seeds, feeds and related aquaculture items (e.g. vaccines) have also been
reported due to restrictions on transportation and travel of personnel,
impacting the aquaculture industry (FAO, 2020b). Drop in Chinese market
due to lockdown has resulted in decrease of fish and seafood consumption
affecting international trade (FAO, 2020b). Growing evidence of unsold
3
https://uonblogs.newcastle.edu.au/bluegreen/murray-darling-citizen-scientists/
CRITICAL REVIEWS IN ENVIRONMENTAL SCIENCE AND TECHNOLOGY 33
produce has resulted in an increase of live fish stocks resulting in higher
feeding costs and greater risk of fish mortalities (e.g. seabass production in
Australia
4
). This pandemic has encouraged the stakeholders of the aquacul-
ture sector (e.g. farmers, feed providers, traders, international agencies,
NGOs, governments) to share information about their situations locally
and internationally. This will enable identification of short-term and long-
term impacts of catastrophic events such as this, as well as the techno-
logical evolution of aquaculture.
Nonetheless, proper planning, management and collaboration of knowledge
and skills on both local and international levels could ensure sustainable devel-
opment of the aquaculture industry and food security in urban areas.
Acknowledgements
We would like to thank the Singapore Food Agency for their inputs, Sidra Aslum from
Fiverr who provided us with the conceptual diagram.
Disclosure of statement
No potential conflict of interest was reported by the authors.
Funding
This study was supported by the National Research Foundation, Prime’s Minister’s Office,
Singapore under its Marine Science Research and Development Programme (Award No.
MSRDP-P13) and NRF-NERC-SEAP-2020 grant call, “Understanding the Impact of Plastic
Pollution on Marine Ecosystems in South East Asia (South East Asia Plastics (SEAP)”
(Award No. SEAP-2020-0003).
ORCID
Aurore Trottet http://orcid.org/0000-0003-2628-6732
Christaline George http://orcid.org/0000-0001-7378-1010
Guillaume Drillet http://orcid.org/0000-0001-5908-0568
Federico M. Lauro http://orcid.org/0000-0002-8373-1014
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