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Management of Biological Invasions (2014) Volume 5, Issue 1: 21–30
doi: http://dx.doi.org/10.3391/mbi.2014.5.1.02
© 2014 The Author(s). Journal compilation © 2014 REABIC
Open Access
21
Research Article
Fouling around: vessel sea-chests as a vector for the introduction
and spread of aquatic invasive species
Melissa A. Frey1*, Nathalie Simard2, David D. Robichaud3, Jennifer L. Martin4 and Thomas W. Therriault5
1Royal British Columbia Museum, 675 Belleville Street, Victoria BC, V8W 9W2, Canada
2Maurice Lamontagne Institute, Fisheries and Oceans Canada, 850 Route de la Mer, Mont-Joli QC, G5H 3Z4, Canada
3LGL Limited, 9768 Second Street, Sidney BC, V8L 3Y8, Canada
4St. Andrews Biological Station, Fisheries and Oceans Canada, 531 Brandy Cove Road, St. Andrews NB, E5B 2L9, Canada
5Pacific Biological Station, Fisheries and Oceans Canada, 3190 Hammond Bay Road, Nanaimo BC, V9T 6N7, Canada
E-mail: mfrey@royalbcmuseum.bc.ca (MAF), nathalie.simard@dfo-mpo.gc.ca (NS), drobichaud@lgl.com (DDR),
jennifer.martin@dfo-mpo.gc.ca (JLM), thomas.therriault@dfo-mpo.gc.ca (TWT)
*Corresponding author
Received: 20 July 2013 / Accepted: 19 November 2013 / Published online: 1 February 2014
Handling editor: Alisha Dahlstrom
Abstract
Sea-chests, recesses built into the hull of a vessel, have been recently identified as hotspots for fouling organisms. In this study, we examined
the types and abundances of taxa found in sea-chests of commercial vessels, and investigated whether vessel specifications and voyage
histories influenced the nature and extent of sea-chest fouling. Eighty-two sea-chests were sampled from 39 commercial vessels while in dry
dock on the West or East Coast of Canada. Overall, 80% of the vessels showed evidence of sea-chest fouling, and 46% harboured at least one
non-indigenous species. In total, 299 unique taxa were recorded, including a number of non-indigenous and cryptogenic organisms that
collectively made up 20.5% and 14.4% of the taxa sampled from West and East Coast vessels, respectively. Additional results suggested that
in-service period (i.e., duration since last sea-chest cleaning) and vessel origin (i.e., domestic versus international) may, in part, determine the
nature and extent of sea-chest fouling. By contrast, vessel size and port duration were unable to explain taxonomic richness or abundance of
fouling organisms in sea-chests. Taken together, these findings highlight the role of sea-chests as an important vector responsible for the
introduction and spread of a variety of taxa, including aquatic invasive species, but also suggest that the factors that influence sea-chest
fouling in commercial vessels are complex. Further research, aimed at better understanding the determinants of sea-chest fouling and the
efficacy of anti-fouling systems, would help further refine management strategies and reduce the risks associated with sea-chest fouling.
Key words: biofouling, biological invasions, dispersal, non-indigenous, seachests, shipping, vessels
Introduction
For centuries, shipping has served as the
principal vector for the introduction and spread
of aquatic invasive species worldwide (e.g.,
Cohen and Carlton 1998; Ruiz et al. 2000; Hewitt
et al. 2004). Historical, slow ocean-going vessels
transported aquatic species that fouled or bored
into the hulls of vessels, likely extending the
distributions of numerous “fouling” organisms
across oceans and along coastlines (Carlton and
Hodder 1995). Today, contemporary shipping is
generally characterized by relatively faster
vessel speeds, shorter port residence times, and
routine hull husbandry, which in turn, may
minimize the extent of biofouling on vessel hulls.
However, given increased levels of global trade,
associated shipping traffic, and new regulations
for anti-fouling agents (e.g., a worldwide ban of
tributyltin (TBT) compounds), biofouling continues
to pose serious invasion risks, particularly if
aquatic organisms are still able to readily
hitchhike from port to port on vessels (Carlton
1996; Gollasch 2002; Minchin and Gollasch 2003).
In addition to the flat surfaces of a vessel’s
hull, there are several specialized ‘niche’ areas
M.A. Frey et al.
22
on which organisms can attach, including bow
thrusters, rudders, propellers, intakes, and sea-
chests. Sea-chests are protected, cavity-like
structures, built into the hull of a vessel and
typically covered with metal grates (Coutts et al.
2003). Despite housing water intakes used for
engine cooling, ballast water operations, and
emergency fire-fighting, sea-chests are typically
characterized by relatively low water flows
compared to higher velocities and shear stresses
experienced on the exposed, flat surfaces of the
hull. Such low-flow environments provide a
relatively protected refuge for many fouling
organisms, leading to increased survivorship and
thriving communities (Coutts and Dodgshun
2007). Indeed, recent studies suggest that sea-
chests and sea-chest grates are hotspots for
biofouling, and by extension, may serve as an
important vector for the introduction and spread
of non-indigenous species (Coutts and Taylor
2004; Coutts and Dodgshun 2007; Sylvester and
MacIsaac 2010).
Anecdotally, sea-chests have been implicated
in the transport and potential spread of several
non-indigenous species, including Mytilus gallo-
provincialis, a well-known invasive mussel that
was found in large numbers in the sea-chests of
an Antarctic supply vessel (Lee and Chown 2007);
Caprella mutica, another widely introduced
species that has spread throughout the North
Atlantic, Northeast Pacific and South Pacific,
possibly as a hitch-hiker in the sea-chests of
commercial vessels (Ashton et al. 2007; Frey et
al. 2009); and Molgula citrina, a North Atlantic
ascidian that recently has been discovered in the
North Pacific, and potentially introduced to the
region via sea-chests (Lambert et al. 2010).
However to date, only a few detailed studies
have quantified the magnitude of biofouling
within sea-chests (Coutts et al. 2003; Coutts and
Dodgshun 2007), thus providing only some of
the information needed to make sound policies
on vector regulation and invasive species
management. The objective of this current study
is to further assess the role of sea-chests as a
potential vector for the introduction and spread
of fouling organisms, including aquatic invasive
species. Specifically, we examined the types and
abundances of taxa found in sea-chests of commer-
cial vessels visiting or operating in Canadian
waters, and whether certain vessel specifications
and voyage histories influenced the nature and
extent of sea-chest fouling.
Methods
Vessel sampling and characteristics
Between 2006 and 2009, we sampled sea-chests
from 39 commercial vessels in dry dock on the
West (n = 25) and East (n = 14) Coasts of
Canada (sampling locations: Victoria, British
Columbia; Les Méchins, Québec; Halifax, Nova
Scotia). For each vessel, we obtained available
data related to vessel specifications and voyage
history by interviewing ship personnel; vessels
with specific data gaps (e.g., unreported port
durations) were sampled but excluded from
respective statistical analyses (see Appendix 1).
Sampled vessels represented a variety of types
and size classes, including barge (n = 2), general
cargo (n = 9), passenger (cruise) (n = 2), ferry (n
= 13), fishing (n = 3), research (n = 9), and tug
(n = 1), and ranged from 139 to 109,000 gross
tonnage (gt). Port duration was estimated as the
average number of days spent in the last five
ports of call (mean = 4.3 days, sd = 4.4, min. =
0, max. = 16.6, n = 30). In-service period was
measured as the number of months since last
inspection and cleaning of sea-chests, including
the complete removal of all fouling organisms.
While the majority of these vessels were in dry
dock for routine maintenance following several
consecutive years at sea, a few ships were
docked for emergency repairs, providing the
opportunity to sample vessels over a broad range
of in-service periods (mean = 29.6 months, sd =
15.5, min. = 0.5, max. = 59.1, n = 28). We
classified vessel origin as ‘domestic’ (n = 23) if
travel occurred exclusively in Canadian waters
(i.e., along each coast), or ‘international’ (n =
16) if the vessel sailed to a foreign port within
the previous five ports visited. Based on
interview responses and visual inspections, all
sampled vessels and associated sea-chests appeared
to have been fitted with cathodic protection
systems (e.g., Cathelco®) and/or treated with anti-
fouling coatings (e.g., Interspeed 640 Red A/F)
to control biofouling. Unfortunately detailed
records for these anti-fouling systems (e.g., type,
location, and age) were unavailable for most
vessels, and therefore not suitable for further
analysis.
Sea-chest sampling and characteristics
Shortly after the arrival of each vessel, we
sampled between one and four sea-chests (mean
= 2.1 sea-chests per ship, sd = 0.8), depending on
Sea-chests as a vector for aquatic invasive species
23
permitted access and time; in total 82 sea-chests
were examined. Preliminary sea-chest surveys
conducted prior to this study (Couture and
Simard 2007) suggested that, in general, fouling
organisms are not evenly distributed within sea-
chests, but rather in patches. To account for
spatial heterogeneity, we implemented a sampling
design that consisted of quadrat sampling, timed
searches, and visual estimates. Within each sea-
chest, three 0.01m2 quadrats were placed on
surfaces with the greatest amount of biofouling,
and all organisms within each quadrat were
collected using a putty scraper (Ardisson et al.
1990). We then conducted timed inspections (5
minutes) to search for rarer taxa potentially not
sampled within the quadrats. To assess whether
the sampled organisms were alive, specimens
were examined prior to preservation in 70%
ethanol. Within each entire sea-chest, we also
relied on visual estimates of percentage cover to
quantify the overall extent of biofouling. To
minimize observer biases on different coasts,
estimates made in the field were later verified by
a single investigator using photos. Although sea-
chests varied in size as characterized by total
surface area (mean = 7.6 m2, sd = 9.5, min. =
0.2, max. = 53.5), this standardized sampling
approach ensured equal sampling effort among
sea-chests. Sea-chest grates were occasionally
sampled by taking scrapings or bulk collections
(taxonomic data available upon request), but
ultimately these samples were not included in the
following analyses.
Classification of taxa
Individuals larger than 1 mm were examined
with dissecting and compound microscopes and
subsequently identified to species or the lowest
taxonomic level possible using available taxonomic
keys and species descriptions (e.g., Carlton
2007). Taxa were further categorized as either
‘indigenous’ (taxa that are native to each respective
coast), ‘non-indigenous (non-established)’ (non-
native taxa that have not been reported previously in
the region), ‘non-indigenous (established)’ (non-
native taxa that are presently established in the
region), ‘cryptogenic’ (taxa of unknown origin),
or ‘unknown’ (taxa that have been identified to
genus or higher, and whose origin remains
unclear). For certain groups, we consulted with
additional taxonomic experts to confirm the
identity and origin of each species (see
acknowledgements). Specimens that appeared
dead upon collection and already represented by
live individuals (e.g., empty shells of mussels
(Mytilus sp.) and tests of barnacles (Balanomorpha))
were excluded from further analyses.
Data analysis
To quantify the extent of biofouling, we
calculated both taxonomic richness (i.e., number
of unique taxa) and abundance (i.e., average
percentage cover) of organisms for each vessel.
We then examined whether either of these measures
were influenced by vessel specifications or voyage
histories. Linear models were implemented to
separately test the effects of each factor:
regression was used to examine vessel size, port
duration, and in-service period, while an analysis
of variance (ANOVA) was used to evaluate
vessel origin. For the purposes of testing the
effect of these factors on taxonomic richness, we
randomly selected a single sea-chest per vessel
to avoid biases that may have been introduced by
uneven sampling of multiple sea-chests among
vessels. To test their effect on abundance, we
used the average percentage cover of all sea-
chests sampled within each vessel. Taxonomic
richness and abundance data were square-root and
arcsine transformed, respectively, to meet statistical
assumptions. We recognize that these factors
could be confounded by complex interactions;
however, data gaps reduced the usefulness of a
full-factorial multiple regression. Analysis of
similarity (ANOSIM) tests, based on Bray-Curtis
similarity matrices calculated from presence/absence
of taxa, were also performed to evaluate
similarities of taxonomic composition between
and within vessels. Separate tests were performed
for each coast, and rather than creating zero-
adjusted coefficients, samples that contained no
species were removed from the analyses (Clarke
and Gorley 2006). Analyses were carried out
using JMP v4.0.2 (SAS Institute) and PRIMER
v6.1.9 (PRIMER-E Ltd.).
Results
Extent of biofouling in sea-chests
Overall, 80% of sampled vessels showed
evidence of sea-chest fouling. The number of
unique taxa found in each sea-chest ranged from
0 to 47 with an average of 8.9 ± 12.1 taxa (mean
± sd); within each vessel, taxonomic richness
ranged widely from 0 to 61 (Figure 1A) with an
average of 14.9 ± 16.8 taxa (mean ± sd). The
extent of biofouling as measured by surface area
M.A. Frey et al.
24
Figure 1. Distribution of A) taxonomic richness (number of
taxa) shown with B) corresponding abundance (average
percentage cover) in sea-chests for sampled vessels. Vessels
ordered by increasing taxonomic richness, and do not correspond
to codes in Appendix 1.
Figure 2. Relationship between in-service period (i.e., duration
since last sea-chest cleaning) and extent of fouling as measured
by: A) taxonomic richness (number of taxa), and B) abundance
(average percentage cover) in sea-chests for each sampled vessel.
Regression line shows back-transformed model fit.
coverage varied from 0 to 90% (Figure 1B) and,
across all vessels, averaged 17.8 ± 24.6% (mean
± sd). Interestingly, vessels with heavily fouled
sea-chests (i.e., high average percentage cover)
did not necessarily equate to those with elevated
taxonomic richness (i.e., large number of taxa)
(Figure 1).
In total, we collected 299 distinct taxa (see
Appendix 2), representing a broad spectrum of
invertebrates, algae, and sea-grass, and including
54 non-indigenous (both non-established and
established) and cryptogenic species. Communities
were dominated by arthropods (primarily
barnacles and amphipods, found in 63% of sea-
chests), molluscs (bivalves and gastropods,
55%), cnidarians (primarily hydrozoans, 45%),
polychaetes (45%), and bryozoans (30%). While
the majority of these taxa were recognized as
indigenous, we also identified a substantial
number of non-indigenous and cryptogenic
organisms that collectively, comprised 20.5% and
14.4% of the taxa sampled from West and East
Coast vessels, respectively (Table 1). Non-
indigenous species were found more frequently
on international vessels (63% of those sampled)
than on domestic vessels (35%). Overall, 46% of
all vessels sampled (43% of West Coast vessels;
48% of East Coast vessels) harboured at least
one non-indigenous species within a sea-chest.
Effects of vessel specification and voyage history
on biofouling
Only a few of the factors related to vessel
specification or voyage history, when analyzed
separately, explained taxonomic richness or
abundance in sea-chests (Table 2). Vessel size
appeared to have a marginally significant effect
on biofouling (p = 0.08); however, when the two
largest vessels (both cruise ships) were excluded
from the analysis this weak effect was not
statistically significant (taxonomic richness: R2 =
0.042, F[1, 34] = 1.480, p = 0.23; abundance: R2 =
0.030, F[1, 34] = 1.043, p = 0.31). Port duration
also had no significant effect on biofouling. By
contrast, in-service period, defined as the number
of months since previous cleaning of sea-chests,
showed a significant positive relationship with
taxonomic richness, but not abundance (Figure 2,
Table 2). For both measures, however, sea-chest
fouling appeared to significantly increase on
vessels with in-service periods greater than 24
months (taxonomic richness: t = -2.509, df = 26,
p = 0.02; abundance: t = -2.110, df = 26, p =
0.04).
Sea-chests as a vector for aquatic invasive species
25
Table 1. Number and percentage of indigenous, non-indigenous (non-established), non-indigenous (established), cryptogenic, and unknown
taxa sampled from the sea-chests of West and East Coast vessels.
West Coast Vessels East Coast Vessels
Origin of Taxa # of Taxa % of Taxa # of Taxa % of Taxa
Indigenous 82 42.1 51 36.7
Non-indigenous (non-established) 26 13.3 14 10.1
Non-indigenous (established) 9 4.6 2 1.4
Cryptogenic 5 2.6 4 2.9
Unknown 73 37.4 68 48.9
Total 201 139
Table 2. Summary of linear model results of the effects of vessel specifications and voyage histories on: A) taxonomic richness (number of
taxa, square-root transformed), and B) abundance (average percentage cover, arcsine transformed) in sea-chests. Effect size for vessel size
(gross tonnage), port duration (average number of days in port), and in-service period (number of months since last sea-chest cleaning) is the
slope (linear regression); effect size for vessel origin (domestic vs. international) is the mean difference (ANOVA). Significance level, α =
0.05.
Factor R2 Effect Size F df (n-2) p
A) Taxonomic richness
Vessel size 0.080 2.61 x 10-5 3.149 36 0.08
Port duration 0.003 0.025 0.079 28 0.78
In-service period 0.183 0.059 5.840 26 0.02
Vessel origin 0.050 0.886 1.946 37 0.17
B) Abundance
Vessel size 0.083 4.55 x 10-6 3.268 36 0.08
Port duration 0.007 -0.006 0.186 28 0.67
In-service period 0.027 0.003 0.724 26 0.40
Vessel origin 0.062 0.172 2.360 36 0.13
Figure 3. Average (± standard error)
number of indigenous, non-
indigenous (non-established), non-
indigenous (established), cryptogenic,
and unknown taxa sampled from a
single sea-chest in domestic and
international vessels. Asterisk
highlights significant difference in
average number of taxa between
domestic and international vessels (p
= 0.01).
The overall effect of vessel origin was not
statistically significant, although international
vessels harboured more taxa (15.2 ± 3.4, mean ±
se) and had a higher average percentage cover
(25.0 ± 8.5) relative to domestic vessels (10.9 ±
3.1 taxa, 13.1 ± 3.4 % cover). Moreover, non-
indigenous (both non-established and established),
cryptogenic, and unknown taxa were on average
more prevalent on international vessels (Figure
3), albeit this difference was only statistically
significant for non-indigenous species (F[1, 37] =
6.74, p = 0.01). By contrast, indigenous taxa
were found in similar numbers on both
international and domestic vessels. Further analysis
(ANOSIM) revealed that taxonomic composition
was more similar within a vessel relative to
among vessels (West Coast: R = 0.59, p = 0.001;
East Coast: R = 0.72, p = 0.001). The same
analyses for vessels grouped by origin suggested
that sea-chests of domestic and international
M.A. Frey et al.
26
vessels did not significantly differ in overall
taxonomic assemblage (West Coast: R = 0.04, p
= 0.22; East Coast: R = 0.04, p = 0.34).
Discussion
Similar to earlier investigations (Coutts et al.
2003; Coutts and Dodgshun 2007), our findings
confirm that commercial vessels can harbour
both an abundance and a diversity of fouling
organisms, including many non-indigenous and
cryptogenic taxa, within their sea-chests. While
the above results indicate that the extent of
biofouling, as measured by both percentage cover
and taxonomic richness, is quite variable across
vessels, the frequency of biofouling, as estimated
by the percentage of vessels with sea-chest
fouling, is relatively high with 80% of the
sampled vessels exhibiting some level of biofouling.
In general, these findings are consistent with the
few other studies that have quantified fouling in
sea-chests or on sea-chest gratings, and highlight
the role of this niche area as a hotspot for
biofouling (Coutts and Taylor 2004; Coutts and
Dodgshun 2007; Sylvester and MacIsaac 2010).
The number of non-indigenous species found
in this study further underscores the notion that
sea-chests pose a serious risk for the introduction
and spread of aquatic invasive species (Coutts
and Dodgshun 2007). On both coasts a sizeable
proportion (~15–20%) of the sea-chest community
was identified as non-indigenous or cryptogenic.
These results are lower than those reported in a
recent hull fouling study that also sampled
vessels on both coasts of Canada (~40-46%)
(Sylvester et al. 2011); however, it is important
to note that this latter investigation focused on
international vessels only. By contrast, our estimates
are comparable to those found in a similar sea-
chest study (~25%), which surveyed both
international and domestic vessels (Coutts and
Dodgshun 2007). In addition to these findings,
nearly half of all vessels sampled here carried at
least one non-indigenous species within their
sea-chests. We documented a number of non-
indigenous taxa that have already successfully
invaded other areas of the world, and may be
well-adapted to the temperate waters of Canada.
For example, the gammarid amphipod Elasmopus
rapax was found in significant numbers (>1,500
individuals/m2) in the sea-chests of an international
vessel arriving from Hawaii to the West Coast of
Canada. This small amphipod has been reportedly
introduced in Hawaii (Coles et al. 1999; but see
Hughes and Lowry 2010), California (Chapman
in Carlton 2007), and in temperate ports throughout
southern Australia (Hughes and Lowry 2010).
Similarly the bryozoan Bugula neritina, a well-
known fouling organism widely introduced and
expanding on both coasts of North America (e.g.,
Cohen and Carlton 1995; Pederson et al. 2005),
was discovered in the sea-chests of an international
vessel that had traveled extensively throughout
the Atlantic prior to arrival on the East Coast of
Canada. Given these invasion histories, such
fouling species seem primed for establishing
populations in the temperate waters of Canada;
and based on our observations, sea-chests could
serve as the primary vector of introduction for
these non-indigenous species.
Sea-chests may also play an important role in
the secondary spread of already established non-
indigenous or cryptogenic species. During this
study, we discovered large numbers (100–4,300
individuals/m2) of the invasive caprellid amphipod
Caprella mutica in the sea-chests of several
domestic vessels, each exclusively operating in
the West Coast or in the East Coast of Canada.
While we proposed that sea-chests may have
facilitated the spread of this species, at least
along the West Coast (Frey et al. 2009), a similar
argument may hold for many of the other non-
indigenous and cryptogenic species found in the
sea-chests of domestic vessels, including the
invasive tunicate Ciona intestinalis – a species
already present on both coasts of North America
and whose spread is of concern to managers and
policy-makers (Therriault and Herborg 2008;
Locke et al. 2009). The above results confirm
that the sea-chests of international vessels are
more likely to harbour non-indigenous species
(and more of them). However once established,
domestic vessels may play an equally significant
role by spreading these species via intra-coastal
voyages (Simkanin et al. 2009; for examples
from recreational boats, see Clarke Murray et al.
2011; Lacoursière-Roussel et al. 2012).
Previous investigations have demonstrated that
certain factors, related to vessel specifications and
voyage histories, likely play a major role in
contributing to the nature and extent of biofouling
(e.g., Coutts and Dodgshun 2007; Davidson et al.
2009; Sylvester and MacIsaac 2010). Accordingly,
we expected vessels with longer port durations
and longer in-service periods to show increased
taxonomic richness and abundance. However, we
found no significant relationship between port
duration and the extent of biofouling in this
study, and contrary to prediction, observed relatively
high levels of sea-chest fouling in some vessels
Sea-chests as a vector for aquatic invasive species
27
that had brief port residency times (e.g., averaging
one day or less). Admittedly the available data
was limited to the last five ports, and may not
accurately reflect typical port durations since last
dry docking. As an additional caveat, it is important
to note that anti-fouling systems were not evaluated
in our analyses, and may have confounded some
of our findings. By contrast, in-service period
did appear as an important determinant for sea-
chest fouling, which is consistent with other
biofouling studies (Coutts 1999; Davidson et al.
2009; but see Sylvester and MacIsaac 2010). On
average, vessels operating for more than approxi-
mately 24 months since last dry docking had
significantly higher taxonomic richness and
abundance. These results, coupled with comparable
findings from recent hull fouling investigations
(Davidson et al. 2009; Sylvester et al. 2011),
demonstrate that current cleaning and maintenance
practices may not sufficiently control biofouling.
They also suggest that shorter periods between
scheduled maintenance may be an effective
management strategy to prevent excessive levels
of biofouling (Sylvester et al. 2011). Although
we were unable to examine other factors, including
sailing speed, voyage routes, extensive port
history, sea-chest environmental conditions, and
anti-fouling systems due to data limitations, such
factors may be important determinants of sea-
chest fouling (Coutts et al. 2010; Sylvester et al.
2011), and represent vital areas for further
research.
Indeed, a comprehensive understanding of the
factors that significantly influence sea-chest
fouling would likely improve our ability to
identify and manage associated invasion risks.
For example, although vessel origin may not account
for overall taxonomic richness or abundance, our
results show that origin does influence the type
of species that are associated with sea-chests.
International vessels are more likely to harbour
non-indigenous (both non-established and
established) species, and on average, carry signi-
ficantly more non-indigenous (non-established)
species than domestic vessels. In Canada, more
than half of recent commercial shipping traffic is
international (Statistics Canada 2012), with the
majority of West Coast arrivals originating in
Asia or the West Coast of the United States, and
East Coast arrivals coming from the East Coast
of the United States or Europe (Lo et al. 2012).
Lo et al. (2012) also showed that wetted
(immerged) surface area, used as a proxy for
potential propagule pressure of biofouling, was
significantly correlated with vessel arrivals.
However it is important to consider that, as
found with ballast water (Verling et al. 2005),
the large variation of sea-chest fouling among
vessels observed in this study suggests that
invasion risk may not be a simple function of
total vessel arrivals, but rather dependent on a
complexity of factors involving various vessel
specifications and voyage histories. Under-
standing which factors contribute most to sea-
chest fouling remains essential for developing
effective invasion management strategies.
Collectively, our findings support the notion
that sea-chests represent a greater source of non-
indigenous species than previously thought
(Coutts et al. 2003). Vessel biofouling is the
oldest, most important vector contributing to the
introduction and spread of aquatic invasive species,
accounting for more than 40% of all marine
invasions (Hewitt and Campbell 2010). Indeed,
hull fouling has been directly attributed to a large
number of non-indigenous species in different
regions of the world (e.g., Gollasch 2002;
Simkanin et al. 2009; Rocha Farrapeira et al.
2011), and may pose a greater invasion risk than
all other vectors, including ballast water
(Gollasch 2002; but for freshwater environments,
see Sylvester and MacIsaac 2010). Among the
various niche areas along the hull of a vessel,
sea-chests have been identified as a major hotspot
for biofouling (Coutts and Taylor 2004; Sylvester
and MacIsaac 2010), suggesting that this vector
alone may present a significant invasion risk. In
the present study, we found 47 distinct taxa in a
single sea-chest, comparable to the maximum
taxonomic richness reported in a similar
investigation (Coutts and Dodgshun 2007). By
sampling a second sea-chest in the same vessel,
richness increased to 61 distinct taxa, a level
comparable to that found in more general hull
fouling studies (Drake and Lodge 2007; Sylvester
and MacIsaac 2010). Admittedly, these numbers
represent maximum levels recorded; however, it
has been argued that such extreme cases likely
pose the greatest invasion risk (Drake and Lodge
2007; Sylvester and MacIsaac 2010). We note
that sampling additional sea-chests and vessels
would likely result in increased taxonomic
richness, as species accumulation curves (not
presented here) have yet to reach an asymptote.
Moreover, the ANOSIM results showed that
biotic communities in sea-chests are more
similar within vessels than among vessels,
suggesting that each vessel may deliver a relatively
unique assemblage of organisms to recipient ports.
Vessels with such rich fouling communities can
M.A. Frey et al.
28
rival those found in ballast water (Drake and Lodge
2007), further underscoring the relative importance
of sea-chests as a major vector for aquatic
invasive species.
Despite the associated invasion risks, relatively
few policies and management strategies are
currently in place to regulate sea-chests and other
vectors of biofouling. Certain regional guidelines
have been developed by some governments
(Hewitt and Campbell 2007), but a more global
approach that controls biofouling across all regions
and all vessels has not been implemented yet.
While mandatory regulations for ballast water
management may have reduced invasion risk
(albeit not completely, Bailey et al. 2011), a lack
of comparable strategies for hull and sea-chest
fouling allows for continued transport of biota
and potential shipping-mediated biological invasions
(Davidson and Simkanin 2012). Developing
effective vessel fouling management strategies is
essential, particularly given emergent trends in
shipping activity (e.g., increased port residency
for vessels during global economic downturns)
and recent changes to regulations of anti-fouling
coatings (e.g., ban of TBT), each of which may
ultimately lead to increased levels of vessel
fouling across the globe (Floerl and Coutts 2009;
Piola and Hopkins 2012). In this study, all
vessels reportedly employed an anti-fouling
system to control biofouling within sea-chests
(e.g., cathodic protection systems and/or anti-
fouling coatings). Yet similar to other investigations
(Coutts and Taylor 2004; Coutts and Dodgshun
2007; Davidson et al. 2009), biofouling was still
substantial in some cases, suggesting that current
treatments are not always effective. Even the most
commonly employed marine growth prevention
systems (i.e., sacrificial anodic copper dosing
(Cathelco®) and electrochlorination (Chloropac®))
have operational limitations that in turn can
influence efficacy (Grandison et al. 2011). Thermal
treatment that uses heated seawater offers promise
as an alternative method to control biofouling
within sea-chests; however, this technology needs
further refinement before being implemented
under actual conditions (Piola and Hopkins 2012).
In conclusion, sea-chests serve as an important
vector for the introduction and spread of aquatic
invasive species. Indeed, sea-chests can rival
other major transfer mechanisms such as ballast
water, and similarly, would benefit from the
development of effective biofouling management
strategies. To promote a comprehensive approach
to the control of vessel fouling, the International
Maritime Organization recently outlined voluntary
guidelines centered on management plans, docu-
mentation, inspections, maintenance, anti-fouling
systems, and new design and construction (IMO
2011). These include practical recommendations
for managing sea-chests and other niche areas,
including the installation and upkeep of anti-
fouling systems (e.g., marine growth prevention
systems or thermal treatment systems). Following
the adoption of these guidelines, it will be
important to assess whether the voluntary measures
translate into increased prevention of vessel-
mediated biological invasions (Baily et al. 2011).
For example, just prior to mandatory regulations
in the United States, voluntary compliance with
ballast water management guidelines was relatively
high among vessels that reported; but overall
compliance remained unknown due to vast under-
reporting (Miller et al. 2005). Fortunately, education
and inspection programs appear to result in
increased compliance and improved management
practices (Baily et al. 2011). Additional research,
aimed at better understanding the factors that
influence sea-chest fouling and testing the efficacy
of anti-fouling systems, will help further refine
management strategies and reduce the invasion
risks associated with sea-chest fouling.
Acknowledgements
We thank the following for logistical and technical support:
Transport Canada, Public Works and Government Services
Canada (Esquimalt Graving Dock), Victoria Shipyards, Esquimalt
Drydock, Canadian Maritime Engineering, Point Hope Maritime,
Halifax Shipyards, Verreault Navigation, Ocean Drydock,
shipping companies and crew, Biologica Environmental Services,
C. Carver and A. Mallet (Mallet Research Services), I. Bérubé, R.
Brown, J.-Y. Couture, I. Davidson, M. Galbraith, M. Huot, S.
Lindstrom, D. Mackas, N. Pellegrin, C. Simkanin and D. Sephton.
We especially thank L. Treau de Coeli and B. Ranns for their
assistance in the field and the lab, and J. Carlton, I. Davidson, H.
Gartner, A. Locke, C. Simkanin, and the reviewers for helpful
discussions and comments. Funding for this research was granted
by Fisheries and Oceans Canada’s Aquatic Invasive Species
Program; MAF was supported as a post-doctoral researcher
through the NSERC Visiting Fellowship in Canadian Government
Laboratories Program.
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Supplementary material
The following supplementary material is available for this article:
Appendix 1. Supplementary data for vessels and sea-chests sampled.
Appendix 2. Non-indigenous (including non-established and established), cryptogenic, indigenous, and unknown taxa found in the sea-
chests of vessels sampled while in dry dock on the West Coast and East Coast of Canada.
This material is available as part of online article from:
http://www.reabic.net/journals/mbi/2014/Supplements/MBI_2014_Frey_etal_Supplement.pdf
