Biofouling is a major vector in the transfer of non-native species around the
world. Species can be transported on virtually all submerged areas of ships
(e.g. hulls, sea chests, propellers) and so antifouling systems are used to
reduce fouling. However, with increased regulation of biocides used in
antifoulants (e.g. the International Maritime Organization tributyltin ban
in 2008), there is a need to find efficient and sustainable alternatives.
Here, we tested the hypothesis that short doses of low salinity water could
be used to kill fouling species in sea chests. Settlement panels were
suspended at 1.5 m depth in a Plymouth marina for 24 months by which time
they had developed mature biofouling assemblages. We exposed these panels to
three different salinities (7, 20 and 33) for 2 hours using a model sea
chest placed in the marina and flushed with freshwater. Fouling organism
diversity and abundance were assessed before panels were treated, immediately
after treatment, and then 1 week and 1 month later. Some native ascidian
Biofouling is a major vector in the transfer of non-native species around the world (Carlton et al., 1995; Ruiz et al., 1997; Gollasch et al., 2002; Coutts and Taylor, 2004; Castro et al., 2017). Species can be transported on virtually all submerged areas of ships so antifouling systems are used. However, some areas of ships hulls, such as sea chests and chain lockers, are difficult to access and coat with antifoulants. Consequently, these areas often get heavily fouled by a wide variety of marine organisms such as hydroids, serpulid polychaetes, barnacles, mussels, bryozoans and tunicates (Coutts and Taylor, 2004; Murray et al., 2011).
Non-native species introduction and spread is increasing, e.g. due to the opening of new trade routes, climate change and the increasing speed of vessels. The International Maritime Organization (IMO) decided to tackle this problem initially by adopting a set of voluntary regulations. In 2011, the IMO Marine Environment Protection Committee issued Resolution MEPC.207(62) outlining measures to minimize the risk associated with ship biofouling. These regulations are directed at many stakeholders (e.g. states, shipmasters, operators and owners, shipbuilders, port authorities, ship repair, dry-docking and recycling facilities, and antifouling paint manufacturers and/or suppliers). Two subsequent sets of guidance on biofouling have since been released: one for recreational craft less than 24 m in length (MEPC.1/Circ.792, 2012), and the second evaluating the 2011 guidelines for the control and management of ship biofouling to minimize the transfer of invasive aquatic species (MEPC.1/Circ.811, 2013; Castro, 2014).
Following the Ballast Water Convention in 2017 coming into force, it seems probable that ship biofouling may soon become the subject of a new international treaty. In May 2017, a programme called “Building Partnerships to Assist Developing Countries to Minimize the Impacts from Aquatic Biofouling” (or “GloFouling Partnerships”) was approved by the Global Environment Facility to be implemented by the United Nations Development Programme and executed by the IMO. An implementation phase is scheduled to start in the second half of 2018 and last for 5 years (IMO Circular Letter No. 3768). In some countries, biofouling management plans and record books are already in place as part of national regulations (e.g. in the United States of America, Australia and New Zealand). For instance, in the state of California (USA), ship owner or operators of vessels of 300 gross tons or larger need to submit a hull husbandry reporting form (Scianni et al., 2013).
Biofouling increases shipping operational costs and fuel consumption due to frictional drag: even microbial fouling, which is a precursor to macrofouling, has an effect. There are also the costs of hull cleaning and painting (Schultz et al., 2011; Dobretsov et al., 2013; Davidson et al., 2016). Some organisms (e.g. bryozoans and algae) are tolerant to antifouling compounds and can grow on freshly applied antifouling paint, and are subsequently used as a substratum for other species (Murray et al., 2011). With the ban of tributyltin in 2008, other antifouling systems started to be used, copper-based antifouling being the most commonly used nowadays. Apart from copper, booster biocides are also used in antifouling system despite their potential impacts on the marine ecosystems (Faÿ et al., 2010; Price and Readman, 2013). Glycerophospholipids from soybeans, for instance, are considered effective booster biocides in antifouling paint (Batista et al., 2015). Antifouling compounds from marine bacteria, cyanobacteria, fungi and eukaryotic organisms have also been developed as biocides (Dobretsov et al., 2013). In terms of mechanical tools to remove biofouling, Hearin et al. (2016) showed that mechanical grooming is helpful in reducing fouling on submerged surfaces coated with fouling-release coatings.
Niche areas on vessel hulls (e.g. gratings and propellers) represent a great challenge to minimizing biofouling. On larger vessels, sea chests maximize seawater inflow (e.g. for internal cooling systems and ballast water). These box-shaped structures are difficult to access and coat, they have edges and welds that provide sheltered areas for organisms to settle and recruit (Coutts and Dodgshun, 2007). In Canada, a study of 82 sea chests from commercial ships showed that 80 % of them had fouling organisms and that almost half had non-native species (Frey et al., 2014).
Setting biosecurity goals and implementing measures for controlling
non-indigenous species helps to avoid their spread (Collin et al., 2015). In
order to control biofouling in niche areas on ships, a simple and efficient
treatment method is needed. Numerous methods are available, for example
ultraviolet light (Titus and Ryskiewich, 1994), heated water and steam,
(Leach, 2011; Piola and Hopkins, 2012; Growcott and Georgiades, 2016), or
soaking areas in acids (e.g. acetic acid) or alkalines, such as hydrated
lime (Rolheiser et al., 2012). In Alaska, the invasive colonial ascidian
Given the importance of biofouling as a vector in the world transfer and spread of non-native species, this study tested the hypothesis that a rapid change in the salinity can kill fouling species taking into account the regulation of the osmotic pressure between the surrounded aquatic environment and the organisms body fluids, and offers a simple and efficient biosecurity management tool to minimize biofouling in ship sea chests. This case study was conducted in southwestern England and is representative of the fouling community of the northeastern Atlantic Ocean.
An experiment was conducted in two phases: the first in November 2016 and
the second in July–August 2017 in Millbay marina (50
A model sea chest was built to find out the lowest steady salinity that
could be achieved when the chest was flushed with freshwater whilst
submerged and open to surrounding seawater. The sea chest was a
polypropylene 80 L container (external dimensions:
Polyvinyl chloride (PVC) settlement panels (each
Panels were subjected to one of the following salinity treatments: 7, 20 or
control (33) for 2 hours (five panels per treatment). The lowest salinity
(7) was chosen as it was the lowest steady value achieved inside our
simulated sea chest. The exposure time was chosen based on the studies
conducted by Moreira et al. (2014) and Jute and Dunphy (2017). On the day before
the experiment started, water from the marina was collected and stored at a
constant room temperature of 16
An acrylic
Data from fouling communities were entered into PRIMER-E for abundance analysis and were square root transformed prior to clustering analysis according to Clarke et al. (2016).
The first phase of the experiment was to ascertain the lowest salinity that
could be maintained inside our simulated sea chest. The salinity was
initially 32, decreasing to 24 after 25 min, to 9 after 60 min before
stabilizing at 7 at 86 min. Once the freshwater supply was switched off, the
salinity inside the sea chest increased slowly over a 5 h 20 min period
to 27.3, when the recordings ended. During this time (November), the water
temperature varied between 13 and 13.6
Biofouling communities were similar on panels before and immediately after treatment but thereafter there were marked differences since low salinity treatments killed most of the organisms present. Cluster analysis of the biofouling community composition 1 week after the treatment showed that panels submitted to the same salinity treatment were clustered together, as they had similar communities present. Tight clustering was found for panels exposed to the 7 salinity treatment; few mortality effects were found at 20 salinity and no effects were found on control panels (33 salinity) (Supplement).
On panels treated with 7, terebellid worms quickly disintegrated and the
erect bryozoan
In the salinity 20 exposures,
One month after exposure to the three salinity treatments there were still very clear differences among the treatment groups although some recolonization had begun on the salinity 7 treatment panels (Table 1). Numbers of species and the Shannon–Wiener diversity index show a decrease in diversity after 1 week and a small increase after 1 month for panels exposed to the salinity 7 treatment (Fig. 2).
We obtained a steady salinity value of 7 inside our model sea chest when immersed at Millbay marina while flushed with freshwater. This was the minimum salinity we used in an experiment to assess the mortality of fouling organisms attached to PVC panels when exposed to three different salinities – 7, 20 and 33 (control). The salinity 7 treatment was highly effective at killing most of the macrobenthos on the panels, whereas communities exposed to 20 and 33 were largely unaffected. There was some recolonization of bare substrata on the panels after 1 month, thus this treatment would be best carried out on sea chests before a vessel leaves port, if she is destined for another biogeographic region.
Average number of biofouling individuals per panel subjected to treatment with salinities of 7, 20 and 33 (control), showing % change in abundance after 1 week and after 1 month.
Freshwater exposure is an efficient way of controlling sublittoral marine
fouling organisms as most suffer osmotic stress (Moreira et al., 2014;
Quinton, 2014; Minto, 2014; Jude and Dunphy, 2017). Most organisms were
killed by our two hour treatment with a salinity of 7. For example, although
Of the two most common species found in this study,
Very high levels of mortality occurred in mature biofouling communities
subjected to 2-hour treatment with a salinity of 7, although some
The data set is part of an ongoing PhD project and not currently available in a public repository.
The supplement related to this article is available online at:
MCTdC concieved the experiment design and development, and worked on the species identification, data analysis, manuscript writing and final draft; TV conceived the experiment design, contributed to the experiment development, the species identification and manuscript writing; AY contributed to the species identification and manuscript writing; TF contributed to the experiment development and manuscript writing; JH-S contributed to the data analysis, manuscript writing and critical revision.
The authors declare that they have no conflict of interest.
This article is part of the special issue “Shipping and the Environment – From Regional to Global Perspectives (ACP/OS inter-journal SI)”. It is not associated with a conference.
This study is part of a PhD research grant funded by the National Council for Scientific and Technological Development – CNPq (grant award 200026/2015-1), an agency linked to the Ministry of Science and Technology, in charge of the “Science without Borders Programme” with support from the Directorate-General for Nuclear and Technological Development and the Directorate of Ports and Coasts of the Brazilian Navy. Edited by: David Turner Reviewed by: two anonymous referees