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Asian Fisheries Science 31S (2018): 168–181
Asian Fisheries Society
Aquaculture Biosecurity Challenges in the Light of the Ballast
Water Management Convention
G. DRILLET1,2,*, G. JUHEL3, A. TROTTET1, H. EIKAAS1,4 and J. SAUNDERS1,5
1DHI Water & Environment, Singapore
2SGS Testing & Control Services, Singapore
3Tropical Marine Science Institute National University of Singapore, Singapore
4 DairyNZ, Otago, New Zealand
5 Singapore ETH Centre, ETH-Zurich, Singapore
Shipping plays a crucial role in supporting global trade, including the transport of products
from the aquaculture industry. However, ships may also unintentionally transport invasive species
and pathogens in their ballast water which pose biosecurity risks for aquaculture. The Ballast Water
Management Convention was developed to manage the biosecurity risks posed by ballast water and
has entered into force in September 2017. The management measures and technologies arising from
the convention provide some solutions and opportunities for the aquaculture industry. Among these
is the potential transfer of treatment technologies between shipping and aquaculture in order to deal
with bio-invasion and biosecurity. However, there are residual weaknesses in the regulatory regimes
for ballast water management which may reveal a continuous risk from shipping to the aquaculture
industry. Gaps include knowledge and management of other aquatic bacteria or viruses that could
cause outbreaks in the aquaculture industry and threaten food security and human health. Solutions
include focused risk assessments for aquaculture and regional collaboration.
Keywords: compliance, invasive species, pathogens, regulation, shipping, water treatment
Shipping is one of the key stakeholders of global trade and plays a crucial role in transporting
more than 90 % of all international goods across the globe (Wan et al. 2016). Altogether, there are
more than 50 000 merchant ships sailing the world’s oceans, and this represents a global tonnage of
600 million tonnes (Globallast 2016).
*Corresponding author. E-mail address: Guillaume.Drillet@SGS.com
169 Asian Fisheries Science 31S (2018): 168–181
Naturally, this global trade also includes the trade of fish meals, animal feeds and aquaculture
products. Nearly 40 % of fish output (wild caught and farmed) is traded internationally, making
seafood one of the most extensively traded commodities in the world. It is considered that exports of
fish products from developing countries represent a larger proportion of total exports compared to
that of tropical beverages, nuts, spices, cotton and sugar combined (Asche and Khatun 2006). In this
respect, the aquaculture industry is dependent on the capacity of shipping to transport these goods
and products, and at reasonable prices. There is however, another linkage between these two
industries, and that is the biosecurity risks posed by the global movement of ships which may
unintentionally transport pathogens with the potential to affect aquaculture. There is a need to
understand and evaluate how these two industries are inherently connected. In this paper, we offer
an overview of the existing regulatory regimes developed by the member states participating in the
global objectives of the International Maritime Organization (IMO) as well as the United States of
America's Coast Guard to decrease the risks of transfer of pathogens. We focus on the management
tools and frameworks dealing with the risks associated with the transport of ballast water and
eventually reflect on the potential transfer of technologies between shipping and aquaculture in
order to deal with bio-invasion and biosecurity.
History of Bio-Invasions Associated with Shipping
Invasive species are viewed as a major threat to aquatic ecosystems and have been reported to
affect global economies and societies (Carlton 2002; Occhipinti-Ambrogi and Savini 2003). In the
United States of America alone, the impact of aquatic invasive species is estimated to range between
millions and billions of dollars annually (Lovell et al. 2006). The shipping industry has been
identified as a major source of transport of exogenous species across ecosystems, with about a third
of the introductions due to fouling on ships' hulls and another third due to ballast water exchanges
(Gollasch 2006, 2007; Galil et al. 2014). Aquaculture as a whole represents the other major source
of invasions, and approaches to diminish these risks have been proposed (Leung and Dudgeon
2008). The impacts of shipping on the occurrence of biological invasions was recognized over 100
years ago, when the first suggested introduction of a non-indigenous marine species, the diatom
Odontella sinensis, known from the tropical and subtropical coasts of the Indo-Pacific, was reported
in European waters where it produced dense plankton blooms in the North Sea and more recently in
the Baltic Sea (Olenina et al. 2009). Unlikely to have been carried by ocean currents from such
distant seas, Ostenfeld (1908) suggested that this species was introduced by shipping as part of the
biofouling community on a vessel’s hull or discharged with the water or sediments contained in
ships’ ballast tanks. Later, other phytoplankton species such as toxic dinoflagellates were also
demonstrated to be transported via ballast water (Hallegraeff and Bolch 1992). This is also the case
for species of zooplankton, for which Acartia tonsa, for example, was first described in Europe in
1927 and for which haplotypes were found in the Baltic Sea that were 100 % similar to specimens
from Rhodes Island, United States of America (Rémy 1927; Drillet et al. 2008).
Asian Fisheries Science 31S (2018): 168–181 170
Fortunately, not all species can survive the transfer through ecosystems in tanks or on ship
hulls; and those surviving the transfer may not become invasive. In order to be successful at
invading a new area, an exogenous species must first be pumped into ballast water tanks or
colonialize the hull of a ship; it must survive transportation to a new location where it would be
either discharged or would release offspring; then it must be able to colonize the new ecosystem and
establish itself to the point that it becomes considered invasive (Carlton 1985; Smith et al. 1999).
There is a broad principle that estimates that only 10 % of all potential invasive species make it to
the next step of this succession (Williamson et al. 1986; Williamson and Fitter 1996; Boudouresque
and Verlaque 2002; Coutts et al. 2010).
However, aquaculture pathogens are particularly of concern because they usually remain
unnoticed until disease outbreaks are recognized, by which point they have already affected a
multibillion dollar industry (Minchin 2007; FAO 2016). Furthermore, there is clear evidence of the
role of ships in spreading protozoans, bacteria and viruses to different world regions in ballast water
and sediments, as well as in biofilms on ballast tank surfaces (Drake et al. 2007) and ship hulls
(Sylvester et al. 2011). As most aquaculture activities are usually in the vicinity of ports and quite
often create nutrient-rich sediments, there is a possibility of transfer of pathogens from ballast water
to aquaculture facilities. For example, the human pathogen Vibrio cholerae was released by ships’
ballast waters in Mobile Bay, United States of America in 1994 and led to the poisoning of oysters,
which were subsequently taken off the market for a period of time, leading to significant economic
losses (McCarthy and Khambaty 1994). Other famous cases include the spread of the parasite
Bonamia ostreae or bonamiosis along the south coast of Britain, potentially via barges fouled with
infected native oysters (Ostrea edulis) (Howard 1994). Vertical transmission of certain molluscan
diseases such as Perkinsis spp. have also been observed as a result of the fouling of ships’ hulls by
contaminated commercial molluscs (Gollasch 2002). Contamination via biofouling communities has
also been held responsible for the spread of amoebic gill disease (Neoparamoeba pemaquidensis) in
cultured Atlantic salmon (Tan et al. 2002).
Ballast Water as a Vector of Concern
As previously mentioned, global trade is heavily dependent on the import or export of raw
materials such as wood products, grains, coal, iron and other minerals. These commodities are
transported across the oceans in specialized bulk carrier ships in one direction, taking on ballast
water for their return voyages when not carrying goods. Although ship owners try to transfer goods
during voyages from and to different ports to avoid travelling empty, there is often a need to balance
cargoes in weight. Other ship types such as container vessels may adapt their ballasting regime to
the amount and type of cargo in each port visited through a route across the globe. Ballast water is
used in ships as a means to stabilize the ship when no or limited cargo is present (Fig. 1). It is an
important aspect of the routine activities on-board and ensures that the ship and the crew are safe.
Because of this vital role, ships will to continue to use ballast water for many more decades, if not
171 Asian Fisheries Science 31S (2018): 168–181
Fig. 1. Cross-section of ships showing ballast tanks and ballast water cycle. (Adapted from GloBallast 2016).
Because of the consequences of bio-invasions generated by the exchange of ballast water
across ecosystems, this topic has received quite a bit of attention in the last decades, and much
research on organisms transferred through ballast water or its sediments has been carried out
(Carlton and Geller 1993; Eno et al. 1997; Ruiz et al. 1997; Briski et al. 2011; Seebens et al. 2013).
Ballast water is estimated to be responsible for the transfer of between 7 000 and 10 000 different
species of marine microbes, plants and animals globally, each day (Carlton 1999).
The annual amount of ballast water transported is large; estimated to be between 3.5 billion
tonnes (Endresen et al. 2004) and 10 billion tonnes (Gollasch 1998). Large ships such as bulk
carriers may pump 10 000 to 20 000 m3 of water per hour (GloBallast 2016). Relating this to a
traditional pond size in the Asian shrimp industry, this would equate to 1–3 shrimp ponds per hour.
The International Maritime Organization (IMO), with its headquarters in London, has come up with
a list of the ten most unwanted marine species carried by ballast water (Table 1).
Asian Fisheries Science 31S (2018): 168–181 172
Table 1. The International Maritime Organization's top-ten most unwanted species. Note that this list still omits viruses
and bacteria, which may be more problematic for aquaculture.
Vibrio cholerae (various strains)
Cladoceran water flea
Red/brown/green tides of various species
North American comb jelly
North Pacific seastar
European green crab
Ballast Water Management
To address the issue of biological invasions through shipping, the IMO has worked towards
the development of a regulatory regime which provides measures to protect the environment from
bio-invasions. This includes the Guidelines for the control and management of ships' biofouling to
minimize the transfer of invasive aquatic species (Biofouling Guidelines, resolution MEPC.207
(62)), which are intended to provide a globally consistent approach to the management of
In 1991, the Marine Environment Protection Committee (MEPC) of the IMO adopted the
International guidelines for preventing the introduction of unwanted aquatic organisms and
pathogens from ships' ballast water and sediment discharges through the resolution MEPC.50 (31).
A few years later in 1997, the developments and discussion generated from these first guidelines
supported the IMO-MEPC in adopting the Guidelines for the control and management of ships’
ballast water to minimize the transfer of harmful aquatic organisms and pathogen through the
resolution A 868(20). Eventually, the International Convention for the Control and Management of
Ships’ Ballast Water and Sediments was adopted in 2004 through the resolution MEPC.253 (67).
This last resolution is also referred to as the Ballast Water Management Convention, or BWMC. As
a convention and not a guideline, this last is legally binding. The convention was to enter into force
exactly one year after at least 30 countries representing 35 % of the world merchant shipping
tonnage have ratified it (Article 18). In order to prepare for the convention to enter into force, there
has been a large amount of work carried out by IMO (Fig. 2). To support the preparation of
stakeholders to the entry into force of the convention, the GEF-UNDP-IMO GloBallast Partnerships
Programme was developed (Globallast 2016). This programme was initiated in late 2007 and was
intended to be finished in 2012, but has been extended until the spring of 2017.
173 Asian Fisheries Science 31S (2018): 168–181
Following the ratification of the convention by Finland in September 2016, the BWMC has
entered into force in September 2017. The world merchant fleet is now bonded to the convention.
This entry into force will ensure that a good part of the bio-invasion risks associated with ballast
water exchanges will be managed and reduced.
Fig. 2. Developments associated with the preparation of the entry into force of the Ballast Water Management
Convention. (Adapted from Drillet (2016)). BWMC = Ballast Water Management Convention, BWMS TA = Ballast
Water Management System Type Approval, PSC = Port State Control.
In short, from September 2017 to 2024, more and more ships will have to comply with the
convention in that they will have to ensure that every single ship will have a ship-specific Ballast
Water Management Plan (BWMP) describing how the ship is managing its ballast water and its
sediments, an International Ballast Water Management Certificate (delivered by a flag state,
eventually through a recognized organization), and a Ballast Water Record Book, where every
single ballasting or de-ballasting event will have to be reported. The BWMP will in most cases
include the treatment of ballast water using a Ballast Water Management System (BWMS) which
must receive a Type Approval by an administration (see following paragraphs). However, ship(s) on
short-sea voyage(s) between specified ports or locations across international borders may be granted
an exemption from applying ballast water management systems under the convention (regulation A-
4), if it is decided that the risk of transfer of invasive species is acceptable. A risk assessment should
be carried out and Guideline G7 details the recommended process for this. The regulations allow an
exemption to be granted for multiple ships and voyages between specified ports and locations,
thereby supporting a regional approach to exemption through the identification of a “Same Risk
Area” or SRA (Stuer-Lauridsen et al 2018).
Asian Fisheries Science 31S (2018): 168–181 174
Draft guidelines for the risk assessment of a SRA were proposed (Saunders et al. 2016 and
references therein) and were accepted by the MEPC in 2017. Nevertheless, while short-sea shipping
may have a possibility to be exempted of using BWMS, it is expected that most ships will have to fit
or retro-fit a system type approved to treat water.
The Type Approval of Ballast Water Management Systems
In line with the convention, all equipment on-board a ship is type-approved and proven to
work according to a strict set of specifications; BWMS therefore have also to be tested. There are to
date 59 type-approved systems under the IMO umbrella, and the guidelines used for carrying out
these evaluations are referred to as the G8 and G9 guidelines. Globally, there are at least 19
organizations involved in testing BWMS, and these are represented by the NGO Global TestNet
(Global TestNet, 2018).
This network was initially supported through the work of The GEF-UNDP-IMO GloBallast
Partnerships Programme and became independent from this support when signing the Busan
Memorandum of Understanding (MoU) in 2013. The Global TestNet aims to increase levels of
standardization, transparency and openness in testing BWMS. Typically, the BWMS are tested
using volumes of 250 m3 of water through the use of pumps; the water is stored in tanks before
testing the capacity of the BWMS to ensure a valid discharge through a stringent biological
evaluation by an independent laboratory (Fig. 3).
Fig. 3. Top left: the DHI ballast water technology and innovation centre in Singapore, bottom left: cultures of standard
test organisms (Tetraselmis sp.); right: inside a 250 m3 retention tank used for mimicking ballast water transported
during a ship’s voyage.
175 Asian Fisheries Science 31S (2018): 168–181
Similar to the BWMC of the IMO, the United States of America has implemented its own
regulation to deal with the risk management of biological invasions through ballast water. This is
commonly referred as the United States Coast Guard (USCG) regulations, and they became
effective in June 2012 (U.S. Coast Guard. Standards for Living Organisms in Ships’ Ballast Water
Discharged in U.S. Waters. 33 CFR Part 151 and 46 CFR Part 162). Being a national regulation, this
applies only to ships discharging ballast water in United States waters. The discharge standard of
both the USCG and the IMO regulations is similar, and a ship may discharge water containing less
than the following number of organisms:
a) 10 viable organisms per m3 >50 μm;
b) 10 viable organisms per mL between 10 and 50 μm
c) one cfu of Vibrio cholerae per 100 mL or one cfu per 1 g (wet weight) zooplankton;
d) 250 cfu of Escherichia coli per 100 mL; and
e) 100 cfu of intestinal enterococci per 100 mL.
There are some differences between the two regulations, for example, in terms of the
definition of "viability": the USCG regulation considers that an organism discharged in its territorial
waters should be dead, whereas the IMO considers that non-viable organisms should not be taken
into account in the discharge assessment, because of their incapacity to reproduce. Other differences
between the IMO and USCG regulations exist in the guidelines and protocols describing the testing
procedures for granting a type-approval to a BWMS. To date, the USCG has only approved six
systems and more applications are being processed. Yet, this this is seen as a bottleneck by the
shipping industry, who must fit systems onboard ships as soon as possible. The G8 guidelines which
are used as a basis for the testing of BWMS under the IMO umbrella initially presented limitations
because they were developed before any BWMS was ever tested. Some of these limitations have
been raised to the IMO-MEPC, as well as in peer-reviewed papers (Miller et al. 2011; Drillet et al.
2013). In light of these issues, the MEPC has re-opened the G8 guidelines for review and a new
version with a set of more stringent testing obligations was submitted to MEPC, and approved in
October 2016. The revised testing Guidelines G8 are now mandatory (as a code) and this ensures
that no new type-approval will be given to systems tested under the old G8 guidelines after 2018;
and all systems installed on ships after 2020 will be required to be tested under the revised G8
guidelines (the Code). This revision by IMO ensures that the convention will become better at
reaching its objectives of decreasing the rates of bio-invasions.
Remaining Weaknesses, Biosecurity Challenges and Gaps
Although the BWMC provides an important tool for managing the environmental risks from
ships’ ballast water, some stakeholders still consider that the 27 years taken to achieve this has been
too long, that too few states representing the highest tonnage have signed up to the Convention
(Wan et al. 2016) and that gaps remain in the protection measures (Drillet et al. 2016).
Asian Fisheries Science 31S (2018): 168–181 176
The BWMC is an international agreement and therefore only regulates ships exchanging
ballast water across international borders, not wholly within domestic waters. The regulation
applying to ships travelling solely in a single country’s water are specific to that particular country.
The convention therefore creates a scenario where exchange of ballast water between distant ports
of a single country may be unregulated (if not regulated at the national level), while the discharge of
ballast water between ports in neighbouring countries (for example across a strait) is subject to the
regulations set out by the BWMC despite the expected higher ecosystem similarity at the local scale.
For example, in the Southeast Asian context, a ship ballasting on the west coast of Thailand in
the Andaman Sea and travelling to and deballasting in a Thai port in the Gulf of Thailand (ca. 1 500
nautical miles away) would not require an application under the BWMC, while a ship sailing from
Singapore to the island of Pulau Batam (Indonesia), less than 10 nautical miles away, would have to
comply with the convention. This is both biologically and administratively unsound (Stuer-
Lauridsen and Overgaard 2014; Saunders et al. 2016). Currently the only way to resolve such issues
is voluntarily through regional sea approaches and working groups such as the Helsinki Commission
(HELCOM) for the Baltic Sea, OSPAR Commission for the North-East Atlantic sea region and the
Regional Marine Pollution Emergency Response Centre (REMPEC) for the Mediterranean Sea.
Furthermore, while the BWMC will reduce the risks of transfer of organisms larger than
10 μm and of bacteria that are harmful to humans, including Vibrio cholerae, Escherichia coli and
Enterococcus spp., the convention does not mention any other aquatic bacteria or viruses that could
cause epizootics in the US$ 160 billion aquaculture industry and threaten food security and human
health (Drillet et al. 2016). Therefore, it has been proposed that risk assessments should be carried
out and eventually flagged to United Nations (UN) interagencies such as UN-Oceans or GESAMP
(Joint Group of Experts on the Scientific Aspects of Marine Environmental Protection) to
circumvent the potential residual risks which may have been omitted in the BWMC (Drillet et al.
Opportunities: Common Treatment Methodologies
While the gaps outlined above are being addressed, there is also an opportunity for the
aquaculture industry, partly due to the efforts of the shipping industry, to advance the technologies
available for water treatment. The BWMC has permitted the development of a range of technologies
which have been tested in independent test facilities in a robust and controlled manner (see above-
mentioned regulations and guidelines). Some of the technologies developed for the shipping
industry are therefore applicable to aquaculture as well. For a ships' ballast water, the technologies
can be either port-based or ship-based, with the latter being easier to implement because it is more
flexible and ensures that systems are able to function during worldwide operations and capable of
treating very dirty/murky waters (Tsolaki and Diamadopoulos 2010). Ballast water treatment
methods can be categorized as physical separation, mechanical or chemical methods (Tsolaki and
177 Asian Fisheries Science 31S (2018): 168–181
Filtration, either by screen or hydro-cyclone filters, is effective against sediment particles and
a wide range of organisms. Hydro-cyclones require less pump pressure than screen filters and allow
separation of sediments and other suspended solids to approximately 20 μm. Particles or organisms
smaller than this require additional treatment methods.
Thus, filtration or separation treatment is generally run in combination with additional
treatment methodologies such as ultraviolet radiation, heat treatment, electromagnetic pulse
applications, oxidizing and non-oxidizing biocides, and deoxygenation (see review by Tsolaki and
Diamandopoulos 2010). These treatment approaches have also been tested and used in aquaculture
(Otte and Rosenthal 1979; Summerfelt 2003). Therefore, lessons learned in the development of
systems for the shipping industry could be readily transferred to the aquaculture sector in order to
maintain the required high levels of biosecurity in farms (FAO 2010).
Ballast water is a vital aspect of maritime safety, as it ensures the stability and safety of the
ship and therefore protects its crew. The USCG and IMO regulations stand as a cornerstone of the
upcoming achievements from the shipping industry. These regulatory regimes, developed to support
the management of the risks inherently associated with the use of ballast water, will help to reduce
the rate and number of exogenous species transferred across ecosystems. Nevertheless, the
understanding of the risks generated by the exchange of ballast water for the aquaculture industry is
generally low. Limitations in the testing of BWMS have been identified and reveal potential impacts
on human health risk management (Cohen and Dobbs 2015). This may also be true for understudied
pathogens in ballast water tanks and their potential impacts on aquaculture, even after the
installation of BWMS in all ships worldwide (see recent work by Ng et al. 2015; Kim et al. 2015;
and Kim et al. 2016).
There is a gap in our knowledge and a residual weakness in the regulatory regimes for ballast
water management which may reveal a continuous risk from shipping to the aquaculture industry
(Drillet et al. 2016). Until this is evaluated, there are dispositions in the BWMC about the measures
which port states are to take in the event of a bloom of potentially harmful organisms occurring in
their waters and where a ship may ballast water from (regulation C-2). In such cases, port states are
required to inform the ships and eventually propose measures to decrease the risk of ballasting water
containing such organisms in ballast water tanks.
The aquaculture stakeholders may benefit from this disposition by ensuring that countries
monitoring the water quality in their port test for pathogens potentially affecting aquaculture, such
as those reported by the World Organisation for Animal Health (OIE, 2017). Impact assessments of
the risk for aquaculture and marine spatial planning may be used as proper tools to ensure improved
biosecurity (Drillet et al. 2014).
Asian Fisheries Science 31S (2018): 168–181 178
Asche, F. and F. Khatun. 2006. Aquaculture: issues and opportunities for sustainable production and trade. ICTSD
Natural Resources, International Trade and Sustainable Development Series Issue Paper No. 5. International
Centre for Trade and Sustainable Development, Geneva. 63 pp.
Boudouresque, C.F. and M. Verlaque. 2002. Biological pollution in the Mediterranean Sea: invasive versus introduced
macrophytes. Marine Pollution Bulletin 44:32–38.
Briski, E., S.A. Bailey and H.J. MacIsaac. 2011. Invertebrates and their dormant eggs transported in ballast sediments of
ships arriving to the Canadian coasts and the Laurentian Great Lakes. Limnology and Oceanography 56:1929–
Carlton, J.T. 1985. Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water.
Oceanography and Marine Biology: An Annual Review 23:313–371.
Carlton, J.T. 1999. The scale and ecological consequences of biological invasions in the world's oceans. In: Invasive
species and biodiversity management (eds. O.T. Sandlund, P.J. Schei and Å. Viken), pp. 195–212. Kluwer
Academic Publishers, Dordrecht.
Carlton, J.T. 2002. Bioinvasion ecology: assessing invasion impact and scale. In: Invasive aquatic species of Europe.
Distribution, impacts and management (eds. E. Leppäkoski, S. Gollasch and S. Olenin), pp. 7–19. Springer, The
Carlton, J.T. and J.B. Geller. 1993. Ecological roulette: the global transport of nonindigenous marine organisms. Science
Cohen, A.N. and F.C. Dobbs. 2015. Failure of the public health testing program for ballast water treatment systems.
Marine Pollution Bulletin 91:29–34.
Coutts, A.D.M., R.F. Piola, C.L. Hewitt, S.D. Connell and J.P.A. Gardner. 2010. Effect of vessel voyage speed on
survival of biofouling organisms: implications for translocation of non-indigenous marine species. Biofouling
Drake, L.A., M.A. Doblin and F.C. Dobbs. 2007. Potential microbial bioinvasions via ships' ballast water, sediment and
biofilm. Marine Pollution Bulletin 55:333–341.
Drillet, G. 2016. A conceptual Port State Control Decision Support System: DHI-PSCBallast. In: Ballast Water
Management Convention: moving towards implementation. Proceedings of the 6th GEF-UNDP-IMO GloBallast
R&D Forum and Exhibition on Ballast Water Management (eds. J. Matheickal, A. Blonce, J. Alonso and M.
Korcak), pp. 82–86. GEF-UNDP-IMO GloBallast Partnerships, London.
Drillet, G., N. Chan, Z. Drillet, A. Foulsham and A. Ducheyne. 2014. Opinions on the sustainable development of
aquaculture. Journal of Fisheries and Livestock Production 2:118. DOI: 10.4172/2332-2608.1000118.
Drillet, G., E. Goetze, P.M. Jepsen, J.K. Højgaard and B.W. Hansen. 2008. Strain-specific vital rates in four Acartia
tonsa cultures, I: strain origin, genetic differentiation and egg survivorship. Aquaculture 28:109–116.
179 Asian Fisheries Science 31S (2018): 168–181
Drillet, G., C. Schmoker, A. Trottet, M.S. Mahjoub, M. Duchemin and M. Andersen 2013. Effects of temperature on
type approval testing of ballast water treatment systems. Integrated Environmental Assessment and Management
Drillet, G., M.S. Wisz, Y.L. Lemaire-Lyons, R. Baulmer, H. Ojaveer, M.G. Bondad-Reantaso, J. Xu, V. Alday-Sanz, J.
Saunders, C.G. Mcowen and H.S. Eikaas. 2016. Protect aquaculture from ship pathogens. Nature 539:31.
Endresen, Ø., H. Lee Behrens, S. Brynestad, A. Bjørn Andersen and R. Skjong. 2004. Challenges in global ballast water
management. Marine Pollution Bulletin 48:615–623.
Eno, C.N., R.A. Clark and W.G. Sanderson. 1997. Non-native marine species in British waters: a review and directory.
Joint Nature Conservation Committee (JNCC), Peterborough.
FAO. 2010. SOFIA. The state of world fisheries and aquaculture. FAO, Rome.
FAO. 2016. SOFIA. The State of world fisheries and aquaculture. FAO, Rome.
Galil, B., A. Marchini, A. Occhipinti-Ambrogi, D. Minchin, A. Narščius, H. Ojaveer and S. Olenin. 2014. International
arrivals: widespread bioinvasions in European seas. Ethology Ecology and Evolution 26:152–171.
Globallast. 2016 http://globallast.imo.org/ accessed November 2016.
Global TestNet. 2018. http://globaltestnet.org/home/ accessed February 2018.
Gollasch, S. 1998. Removal of barriers to the effective implementation of ballast water control and management
measures in developing countries. International Maritime Organisation, London. 188 pp.
Gollasch, S. 2002. The importance of ship hull fouling as a vector of species introductions into the North Sea.
Gollasch, S. 2006. Overview on introduced aquatic species in European navigational and adjacent waters. Helgoland
Marine Research 60:84–89.
Gollasch, S. 2007. Is ballast water a major dispersal mechanism for marine organisms? In: Biological invasions (ed. W.
Nentwig), pp. 49–57. Springer, Berlin, Heidelberg.
Hallegraeff, G.M. and C.J. Bolch. 1992. Transport of diatom and dinoflagellate resting spores in ships' ballast water:
implications for plankton biogeography and aquaculture. Journal of Plankton Research 14:1067–1084.
Howard, A.E. 1994. The possibility of long distance transmission of Bonamia by fouling on boat hulls. Bulletin of the
European Association of Fish Pathologists 14:211–212.
Kim, Y., T. Aw and J. Rose. 2016. Transporting ocean viromes: invasion of the aquatic biosphere. PLoS ONE
Kim, Y., T.G. AwT.K. Teal and J.B. Rose. 2015. Metagenomic investigation of viral communities in ballast water.
Environmental Science & Technology 49:8396–8407.
Asian Fisheries Science 31S (2018): 168–181 180
Leung, K.M. and D. Dudgeon. 2008. Ecological risk assessment and management of exotic organisms associated with
aquaculture activities. In Understanding and applying risk analysis in aquaculture (eds. M.G. Bondad-Reantaso,
J.R. Arthur and R.P. Subasinghe), pp. 67–100. FAO Fisheries and Aquaculture Technical Paper No. 519. FAO,
Lovell, S.J., S.F. Stone and L. Fernandez. 2006. The economic impacts of aquatic invasive species: a review of the
literature. Agricultural and Resource Economics Review 35:195–208.
McCarthy, S.A. and F.M. Khambaty. 1994. International dissemination of epidemic Vibrio cholerae by cargo ship
ballast and other non-potable waters. Applied and Environmental Microbiology 60:2597–2601.
Miller, A.W., M. Frazier, G.E. Smith, E.S. Perry, G.M. Ruiz and M.N. Tamburri, M.N. 2011. Enumerating sparse
organisms in ships’ ballast water: why counting to 10 is not so easy. Environmental Science & Technology
Minchin, D. 2007. Aquaculture and transport in a changing environment: overlap and links in the spread of alien biota.
Marine Pollution Bulletin 55:302–313.
Ng, C., T.-H. Le, S.G. Goh, L. Liang, Y. Kim, J.B. Rose and K.G. Yew-Hoong. 2015. A comparison of microbial water
quality and diversity for ballast and tropical harbor waters. PLoS ONE 10:e0143123.
Occhipinti-Ambrogi, A. and D. Savini. 2003. Biological invasions as a component of global change in stressed marine
ecosystems. Marine Pollution Bulletin 46:542–551.
OIE. 2017. http://www.oie.int/international-standard-setting/aquatic-code/access-online/. Accessed September 2017.
Olenina, I., S. Hajdu, N. Wasmund, I. Jurgensone, S. Gromisz, J. Kownacka, K. Toming and S. Olenin. 2009. Impacts of
invasive phytoplankton species on the Baltic Sea ecosystem in 1980–2008. HELCOM Indicator Fact Sheets.
Ostenfeld, C.J. 1908. On the immigration of Biddulphia sinensis Grev. and its occurrence in the North Sea during 1903–
1907. Meddelelser fra Kommissionen for Havundersogelser. Ser. Plankton 1. 44 pp.
Otte, G. and H. Rosenthal, H. 1979. Management of a closed brackish water system for high-density fish culture by
biological and chemical water treatment. Aquaculture 18:169–181.
Rémy, P. 1927. Note sur un copépode de l'eau saumâtre du canal de Caen a la mer. Acartia (Acanthacartia) tonsa Dana.
Annales de Biologie Lacustre 15:169–186.
Ruiz, G.M., J.T. Carlton, E.D. Grosholz and A.H. Hines. 1997. Global invasions of marine and estuarine habitats by
non-indigenous species: mechanisms, extent and consequences. American Zoologist 37:621–632.
Saunders, J., G. Drillet and G. Foulsham. 2016. A study on same risk area with regards to Ballast Water Management
Convention Regulation A-4 on exemptions to ships. IMO MEPC70.Inf 21. London, United Kingdom.
Seebens, H., M. Gastner and B. Blasius. 2013. The risk of marine bioinvasion caused by global shipping. Ecology
Smith, D.L., M.J. Wonham, L.D. McCann, G.M. Ruiz, A.H. Hines and J.T. Carlton. 1999. Invasion pressure to a ballast-
flooded estuary and an assessment of inoculant survival. Biological Invasions 1:67–87.
181 Asian Fisheries Science 31S (2018): 168–181
Stuer-Lauridsen, F. and S.B. Overgaard. 2014. Note on same risk area. The Danish Nature Agency, Copenhagen.
Stuer-Lauridsen, F., Drillet G., Hansen FT. and Saunders J. 2018. Same Risk Area: An area-based approach for the
management of bio-invasion risks from ships’ ballast water. Marine Policy 97: 147-155
Summerfelt, S.T. 2003. Ozonation and UV irradiation – an introduction and examples of current applications.
Aquacultural Engineering 28:21–36.
Sylvester, F., O. Kalaci, B. Leung, A. Lacoursiere-Roussel, C.C. Murray, F.M. Choi, M.A. Bravo, T.W. Therriault and
H.J. MacIsaac. 2011. Hull fouling as an invasion vector: can simple models explain a complex problem? Journal
of Applied Ecology 48:415–423.
Tan, C.K.F., B.F. Nowak and S.L. Hodson. 2002. Biofouling as a reservoir of Neoparamoeba permaquidensis (Page
1970), the causative agent of amoebic gill disease in Atlantic salmon. Aquaculture 210:49–58.
Tsolaki, E. and E. Diamadopoulos. 2010. Technologies for ballast water treatment: a review. Journal of Chemical
Technology and Biotechnology 85:19–32.
Wan, Z., J. Chen, A.E. Makhloufi, D. Sperling and Y. Chen. 2016. Four routes to better maritime governance. Nature
Williamson, M.H., K.C. Brown, M.W. Holdgate, H. Kornberg, R. Southwood and D. Mollison. 1986. The analysis and
modelling of British invasions [and discussion]. Philosophical Transactions of the Royal Society B: Biological
Williamson, M.H. and A. Fitter. 1996. The characters of successful invaders. Biological Conservation 78:163–170.