Management of Biological Invasions (2016) Volume 7, Issue 4: 351–363
DOI: http://dx.doi.org/10.3391/mbi.2016.7.4.05
© 2016 The Author(s). Journal compilation © 2016 REABIC
Open Access
Research Article
Marine pests in paradise: capacity building, awareness raising and preliminary
introduced species port survey results in the Republic of Palau
Marnie L. Campbell 1,2, * , Chad L. Hewitt 1,3 and Joel Miles 4
1
National Centre for Marine Conservation and Resource Sustainability, University of Tasmania, Newnham, Tasmania, 7250, Australia
Environmental Research Institute, University of Waikato, Hamilton 3240, New Zealand
3
School of Science, Faculty of Science and Engineering, University of Waikato, Hamilton 3240, New Zealand
4
National Invasive Species Committee, Bureau of Agriculture, Ministry of Natural Resources, Environment & Tourism,
969940 Republic of Palau
2
*Corresponding author
E-mail addresses: marnie.campbell@waikato.ac.nz (MLC), chad.hewitt@waikato.ac.nz (CLH), joelmiles52@gmail.com (JM)
Received: 12 April 2016 / Accepted: 19 July 2016 / Published online: 17 September 2016
Handling editor: Vadim Panov
Abstract
Introduced marine species can have a large impact upon small countries that are reliant on marine tourism. Non-governmental organisations,
such as the World Conservation Union (IUCN), are working with technical experts to implement capacity building and awareness programs
that transfers introduced marine species knowledge to countries in need of aid. The Republic of Palau is reliant on tourism and as such is proactively engaging in this process to ensure that it has the necessary skills to determine and manage its introduced marine species pathways
and vectors. The IUCN with the aid of technical experts implemented a four day training workshop that provided both theoretical and
practical field experience with introduced marine species port surveys. An outcome of this exercise was the detection of 11 introduced
marine species, the training of 10 Palau agencies and two international organisations, and recommendations for future implementation that
will aid Palau to address the problem of introduced marine species within their borders.
Key words: non-indigenous species, non-native species, marine pests, biofouling, biosecurity, environmental management, species criteria,
Pacific Island Countries
Introduction
Within the last two decades research on introduced
species has expanded from a focus on ballast water
mediated transport (e.g., Williams et al. 1988; Carlton
and Geller 1993), to a more holistic view of potential
vectors (e.g., Carlton 2001; Hewitt et al. 2004;
Padilla and Williams 2004; Fofonoff et al. 2003;
Campbell and Hewitt et al. 2013; Williams et al.
2015). Marine invaders have now been detected in
virtually all regions of the world oceans, with
indications that multiple vectors contribute to these
broad-scale distributions (e.g., Hayes et al. 2005;
Hewitt and Campbell 2007). Not all countries have
the capacity to determine the current state of invasions
within their waters or the ability to implement proactive biosecurity measures (e.g., Bax et al. 2003;
Hewitt and Campbell 2007; Nuñez and Pauchard
2010; Azmi et al. 2015a, 2015b). This lack of capacity
has serious biosecurity implications. Of particular
concern is the reliance of a number of small island
states, specifically Pacific Island Countries (PICs),
on their marine environments, to the extent that the
“marine economy” derived from tourism, artisanal and
commercial fisheries and aquaculture contributes
more than 10% of Gross National Income (GNI) in
many instances (Table 1).
The marine economy is a useful term to capture
the direct and indirect benefits derived from marine
based activities to GNI, which need to be examined
in the context of marine biosecurity. Marine economy
activities include more traditional economic drivers,
such as commercial export based fisheries, aquaculture, aquarium species collection, and oil and
gas extraction; as well as subsistence fisheries and
marine based tourism (see Table 1). While traditional
economic drivers have previously been calculated
for contribution to GNI, it is commonly realised that
the ability to capture less traditional aspects in PICs
is limited, resulting in an under-estimation of GNI
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M.L. Campbell et al.
Table 1. Pacific Island countries Gross Domestic Product (GDP), currency, and the percentage “marine economy” component of the GDP,
with the Republic of Palau highlighted by italics (source: Gillett and Lightfoot 2001). * – estimate
Country
Cook Island
Federated States of Micronesia
Fiji Islands
Kiribati
Marshal Islands
Nauru*
Niue
Palau
Papua New Guinea
Samoa
Solomon Islands*
Tonga
Tuvalu
Vanuatu
GDP
$171,599,000
$229,869,864
$3,587,300,000
$74,100,000
$97,311,800
$80,000,000
$14,210,300
$129,601,000
$8,780,800,000
$705,914,000
$1,352,700,000
$251,135,000
$22,044,500
$29,206
contribution (e.g., Gillett and Lightfoot 2001; Gibson
and Nero 2008). For many PICs, fisheries can account
for more than 10% contribution to GNI, with marine
based tourism having an equal or greater share.
Despite a high reliance on the marine environment
and marine resources for economic well-being,
many of these PICs have limited understanding
about introduced marine species and the risks they
pose to their economies. As Nuñez and Pauchard
(2010) have discussed, these developing states have
limited capacity or capability to meet the demands
of marine biosecurity within their domain. To address
this, a number of non-governmental and intergovernmental organisations have established programs to
ensure that all countries have access to information
about marine introduced species (awareness raising)
and can receive expert training (capacity building) to
facilitate regional and international outcomes.
Two examples of this proactive international
stance include: 1) the work undertaken by the Global
Ballast Water Management Programme (referred to
as GloBallast) — a collaboration between the Global
Environment Facility (GEF), United Nations
Development Program (UNDP) and the International
Maritime Organisations (IMO) (IMO 2000a); and 2)
the IUCN’s marine programme (IUCN 2013), with a
third organisation unfortunately closing in 2011 (the
Global Invasive Species Programme [GISP]; BGCI
2011). These organisations have provided training
for introduced species surveys, identification and
taxonomy, risk assessment, ballast water management, and public awareness in a number of countries.
Phase I of the Globallast programme undertook
introduced species port survey training in six countries
352
Currency
NZ$
US$
F$
AUD$
US$
AUD$
NZ$
US$
Kina
Tala
SI$
T$
AUD$
Vt million
Marine component (%)
11.31
4.70
2.34
11.98
7.40
2.12
1.58
2.69
0.56
7.99
0.01
7.13
6.77
0.95
(Brazil, China, India, Iran, South Africa, and the
Ukraine). This training provided basic skills in ballast
water management, ballast water risk assessment,
and taxonomic identification (IMO 2000b). In
general, these initiatives targeted stakeholders such
as universities, museums, navy, and port authorities.
GISP had maintained a broader, all-ecosystem
approach to invasive species providing for example,
public awareness (e.g., invasive species posters),
training workshops, and advice to decision makers
(e.g., Simons and de Poorter 2008). Similarly, the
IUCN provides introduced species awareness raising
in countries such as Chile (e.g., Hewitt et al. 2006),
the Seychelles, and Samoa, and have also undertaken
some targeted introduced species surveys (e.g.,
Tamelander et al. 2009).
One example of the IUCN efforts is a facilitation
and capacity building exercise conducted in the
Republic of Palau (herein referred to as Palau) in
2007 on introduced species port survey methods,
both theoretical and applied. This paper provides an
overview of the exercise, including outcomes derived
from the workshop. The work in Palau involved a
number of different in-country agencies, working with
Australian marine biosecurity experts who provided
training that was facilitated by the IUCN and the
Office of Environmental Response and Coordination,
Palau. The activity in Palau focussed on providing
an awareness of introduced marine species and the
problems they cause, training interested agencies in
port survey techniques and taxonomic sorting, and
introducing the concepts of risk assessment.
One of the main objectives of this work was to
ensure that Palau would receive training in skills that
Introduced marine species in Palau
would allow them to undertake their own introduced
species baseline surveys and establish monitoring
programs, thus ensuring that knowledge transfer
occurred. It is anticipated that follow-up surveys
within Palau will further build capacity and increase
knowledge about introduced marine species in this
region. Outcomes from the training exercise provided
preliminary data on the introduced species present in
the region and associated vectors that may pose a
risk to Palau. This type of information can then form
the basis of informed introduced species management programs.
aim of the developed survey was to detect introduced
marine species through examination of marine biodiversity. Therefore, survey sites were selected based
on likely primary inoculation points (areas with
overseas linkages) and secondary sites with high
frequency of visitation from primary inoculation points
(i.e., secondary transfer locations). In addition, sites
of high environmental, economic or socio-cultural
importance were identified for monitoring.
Upon return from the field a literature search was
undertaken to identify known introduced and cryptogenic species from the region to inform the development of a biosecurity framework specific to Palau.
Materials and methods
Training workshop
Between 25th and 28th July, 2007, 10 Palauan agencies
(Bureau of Marine Resources, Bureau of Agriculture,
CARP Dive Tour Company, Koror State Government,
Office of Environmental Response and Coordination
(OERC), Palau Conservation Society, Palau International Coral Reef Centre, Coral Reef Research
Foundation, Peleliu State Government, Sam’s Tours)
and two international organisations (IUCN, The Nature
Conservancy) were trained in introduced marine
species baseline survey design and techniques,
including undertaking a preliminary survey of
Malakal Harbour, Koror State, Palau, sample sorting
and para-taxonomic species identification. It is
important to note that the para-taxonomic training
was focussed on identifying obvious non-native
species (building capability) and providing knowledge
about where to find taxonomic information, such as
relevant databases or how to contact taxonomic experts.
The supplementary material in this paper provides a
list of taxonomic databases and references that we
typically provide during port survey capacity building
training.
A component of the project included in-water
training of methods and post-survey taxonomic
sorting with species identification. The survey training
specifically covered the Hewitt and Martin (1996,
2001) protocols, with further information provided
during a workshop on alternative protocols such as
the Rapid Assessment Survey (RAS) surveys (e.g.,
Cohen et al. 2001, 2005; Pedersen et al. 2003), the
Bishop Museum protocols (e.g., Coles and Eldredge
2002), the Chilean aquaculture survey protocols (e.g.,
Hewitt et al. 2006), and passive sampling (Ruiz and
Hewitt 2002; Wyatt et al. 2005; deRivera et al. 2005).
Workshop participants designed a baseline survey,
grounded by their shared local knowledge coupled
with their training in the Hewitt and Martin protocols
(1996, 2001). As with all baseline port surveys; the
Survey site
Palau is an archipelago of over 586 islands (eight
main islands) located east of the Philippine island of
Mindanao; the first Europeans to see the islands
were the Spanish in the 1500’s (Faulkner et al. 2004;
Yukihira et al. 2007). It is a biodiversity hotspot
(Faulkner et al. 2004; Yukihira et al. 2007) and a
well-known international tourist destination based
on its Rock Islands, jellyfish lakes and unique
SCUBA diving opportunities (Yamashita 2000). The
government is proactive, with regards to introduced
pests and are concerned with the potential impact
introduced marine species pose to their tourism
(including charter fishing) industries.
Introduced species survey methods
The preliminary survey served two purposes: 1) to
train the survey team in introduced species survey
methods; and 2) to undertake a preliminary examination of the species present in Malakal Harbour. The
survey aimed to detect introduced marine species
and provide an indication of their spatial distribution.
Collection of native biodiversity data was a secondary
aim of the survey plan. Within this paper we discuss
the detection of introduced marine species, not
native species.
An initial suite of survey sites were selected by
introduced species port survey specialists for consideration by the workshop participants. This selection
of sites was subsequently discussed with workshop
participants to add local knowledge and thereby
improve site selection by adding or removing sites
where needed. This ensured that selection of sites
was refined and prioritised based on the heuristic
knowledge of the workshop participants, coupled
with the prioritisation knowledge provided in the
Hewitt and Martin (2001) introduced species sampling
principles (Table 2). At the end of the heuristic
workshop process, a total of 38 sites were identified,
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M.L. Campbell et al.
Table 2. Sites selected for introduced marine species surveys, including method of sampling, heuristic priorities and introduced species
priorities. Italic font indicates sites that would be sampled under a typical introduced marine species survey using the Hewitt and Martin
(1996, 2001) protocols.
Site name
Neco floating dock
Neco marine dock
PMIC
Sam’s Tours
Channel marker
Bureau of Marine Resources/Belau -Mariculture
Demonstration Center
Marine Law Enforcement
Commercial Berth 3 (south)
Commercial Berth end
Method
Training sites covered
Qualitative
Quantitative
Quantitative
Quantitative
Semi-quantitative
Heuristic priority
Introduced spp priority
2
2
1
1
2
1
1
1
1
1
1
1
1
1
1
1
1
1
3
2
2
2
1
1
1
2
2
3
1
1
1
3
2
1
1
1
1
2
1
3
1
4
1
3
3
1
1
1
1
1
3
3
3
2
1
1
2
3
3
3
2
1
1
1
3
3
2
1
1
2
2
1
2
3
1
3
Quantitative
Quantitative
Quantitative
Qualitative
Phase 1 – Malakal port sites
Malakal causeway
Quantitative
Palau Royal Resort
Quantitative
Carp Restaurant
Quantitative
Fisheries wharf
Quantitative
Palau Island Traders International
Quantitative
BRM - mariculture
Quantitative
Marine law
Quantitative
Barge wreck
Qualitative
CPR – dry dock
Quantitative
Chandelier cave
Qualitative
Recreational anchorage
Qualitative
Recreational anchorage – Chinese wreck
Qualitative
Recreational anchorage - wreck
Qualitative
Old Japanese dry dock
Qualitative
Phase 2 – external to port – Koror State
Channel buoys 1
Semi- quantitative
Channel buoys 2
Semi- quantitative
Channel buoys 3
Semi- quantitative
Derelict tugs
Qualitative
Large foreign vessel anchorage Pincher Bay
Qualitative
PPR
Qualitative
Sea plane anchorage
Qualitative
T-dock (historical jetty)
Qualitative
KB (JP) bridge - north
Quantitative
KB (JP) bridge - south
Qualitative
Fish & fins/PICRC
Quantitative
Dump site
Qualitative
Ngetkedam
Qualitative
Anchorage – near helmut dive site
Qualitative
MV “Pristine”
Qualitative
Phase 3 – beyond Koror State (To be designed)
within a three phase program (phase 1 – Malakal Harbor;
phase 2 – surrounding regions within Koror State;
and phase 3 – areas outside of Koror State) being
suggested to complete the site survey. This paper
concentrates on phase 1, with phases 2 and 3 underway
via the Koror Rangers at times of their convenience.
Typically, an introduced species survey for a
region of this size would sample fewer sites (e.g., 22
sites) but retaining the ability to detect low density
invasions (e.g., Hewitt and Martin 2001). Indicated
in Table 2 (via italic font) are the sites that would be
354
sampled during a full Hewitt and Martin style
survey. By sampling fewer sites but maintaining a
high detection limit (statistical ability to find an
introduced species based on the sampling effort
expended), the efficiency of the survey is increased
both with regards to resource use and statistical
robustness. However, when training participants, it
is often desirable to include more sites to ensure the
inclusion of stakeholder opinion.
A number of sites that were sampled through
visual inspection (qualitative sampling) were added
Introduced marine species in Palau
Figure 1. A selection of the survey sites in Palau: Malakal Harbour (A, B), “pristine” areas (C, D), and tourist sites (E, F).
to the survey in an ad-hoc fashion, with introduced
or suspect introduced species being noted at all ad
hoc sites. Samples from the hulls of three vessels
were also collected in a qualitative fashion. Fouling
communities were sampled at 16 sites; nine sites
within Malakal Harbour and seven sites outside of
the harbour, including three “pristine” sites in the
Rock Islands (Figure 1). Standard 0.10 m2 quadrats
were used to sample hard substrate using the methods
described in Hewitt and Martin (1996, 2001).
Quadrats were sampled at three depths (–0.5m, –3m,
and –7m) in triplicate (n = 9 samples) where depth
allowed. When depths were limited (too shallow),
two depths (–0.5m and –3m) were sampled using four
replicates (n = 8 samples). During this preliminary
survey no benthic cores, phytoplankton or pelagic
samples were collected and hence sampling focussed
on biofouling communities.
Collected specimens were placed on ice until
taxonomic sorting and identification occurred on the
afternoon of the day that collection occurred.
Specimens were preserved using 70% ethanol and
355
M.L. Campbell et al.
labels were used to ensure that site and specimen
integrity was maintained following the methods of
Hewitt and Martin (1996). Specimens were identified
to least taxonomic unit, aiming to obtain a species
level identification, so that species status (is it a
native, introduced, cryptogenic species) could be
derived. A number of para-taxonomic experts were
involved in the species identifications.
Identifying a species status
A modified version of the Chapman and Carlton
(1991, 1994) 10-point criteria was used to determine
a species status (Table 3; Campbell et al., in review).
These criteria evaluate ecological, geographical and
evolutionary attributes of a species, using deductive
reasoning to aid in the determination of a species
status. Knowledge that spans across multiple disciplines, such as taxonomy, phylogeny, genetics,
ecology, biology, and biogeography, is used to
assess the species status. The modified criteria have
been trialled (e.g., Brazil, China, India, Iran, Samoa,
the Seychelles) in regions where a historical track
record of native species exist and worked relatively
well (M Campbell, unpublished data).
The modified criteria include an additional five
criteria to those that Chapman and Carlton (1991,
1994) originally suggested. These new additions were
derived by evaluating native and introduced species
patterns from national and international port survey
data sets (Australia, South Africa, Brazil; Pollard
and Hutchings 1990a, 1990b; Hewitt et al. 1999, 2004;
Hewitt and Campbell 2001; Hewitt 2002; Campbell
2003; Campbell et al. 2004; Hewitt and Campbell,
unpubl. data) and readily available international
species data present in the published literature (e.g.,
Cohen and Carlton 1995; Ribera and Boudouresque
1995; Brattegard and Holthe 1997; Zaitsev and Mamaev
1997; Cranfield et al. 1998; Zaitsev and Alexandrov
1998; Coles et al. 1999; Boudouresque and Verlaque
2002; CIESM 2002; Galil et al. 2002; Leppäkoski et
al. 2002; Orensanz et al., 2002; Green and Short
2003; Occhipinti-Ambrogi and Savini 2003; Castilla
et al. 2005). To determine if a species was native,
introduced or cryptogenic, a “weight of evidence”
approach was applied. Three of the new criteria are
based on patterns linked to an introduced species
affinity with mediated transport mechanisms (such
as vessels and aquaculture) that lead to a broader
distribution than may be observed by naturally
dispersing natives and are summarised as:
— Criterion 7: The local (<10’s km) distribution of
the introduced species is wide when compared to
similar native species’ local distributions;
356
— Criterion 8: The regional (100’s – 1000’s km)
distribution of the introduced species is wide
when compared to similar native species’
regional distribution;
— Criterion 10: Introduced species have a
widespread global distribution;
— Criterion 14: Only one sex of a dimorphic species
can be detected. Several introduced species have
been identified where a single sex is detected and
reproduction is limited to asexual means alone.
Founder effects may result in a reduced probability of individuals of both sexes being
introduced to a locale; and
— Criterion 15: This genus is not present in the
country/island/continent (higher taxonomic affinities are lacking).
Results and discussion
Training workshops
A four day workshop was conducted that involved
10 Palauan and two international organisations. The
initial 2 days involved classroom activities, where
participants were trained using a more traditional
style “chalk and talk” information provision session
followed by information transfer with group activities.
During the “chalk and talk” session experts discussed
what introduced marine species are, the different
field survey techniques that exist for detecting
introduced species (sensu Campbell et al. 2007), and
how risk analysis can be used for marine biosecurity
(e.g., Campbell 2008; Campbell and Hewitt 2011, 2013).
Within the group activities a “strawman” model
of a Hewitt and Martin port survey for Malakal and
surrounding regions was provided to participants.
The workshop participants then used their newly
acquired introduced species and survey knowledge,
plus their local knowledge to modify sites and decide
the best sampling techniques for each subsequently
selected site (Campbell and Hewitt 2008). This combined method resulted in participants stating that they
felt confident that they had the skills to understand,
plan and implement a baseline survey for introduced
species with minimal guidance from experts.
The remaining two-days of the workshop involved
field activities where a group of people that would
be involved in undertaking port surveys had in-water
training in the field sampling and laboratory sorting
techniques. This training resulted in nine sites being
surveyed with additional ad hoc collections. The
preliminary survey detected introduced species and as
such is considered to be a successful implementation
of a knowledge and skills capacity building exercise.
Introduced marine species in Palau
Table 3. Criteria used to determine if a marine species is introduced, cryptogenic or native (from Campbell et al., in review). The criteria are
modified from Chapman and Carlton (1991), with the exceptions of new additions, which are highlighted in bold font and shaded background.
Geography
Provincial
Provincial
Provincial
Provincial
Provincial
Provincial
Provincial
Provincial
Global
Global
Global
Global
Global
Global
Global
Criterion
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
Description
Sudden local appearance
Subsequent local spread
Distribution associated with human mechanisms of dispersal
Trophic dependence (and symbioses) on known introduced marine species
Most prevalent in, or restricted to, new or artificial environments
Local distribution restricted compared to native species
Local distribution wider when compared to native species
Regional species distribution wider when compared to native species
Disjunct global distribution
Widespread global distribution
Active dispersal mechanisms are inadequate to attain current global distribution without human aid
Passive dispersal mechanisms are inadequate to attain current global distribution without human aid
The species is most similar morphologically, or genetically, to species in other regions of the world
Only one sex of a dimorphic species can be detected
This genus is not present in the country/island/continent (higher taxonomic affinities are lacking)
Baseline survey results
The preliminary field survey detected 11 introduced
and two cryptogenic and seven potentially introduced
species (Table 4). The introduced species were
dominated by bryozoans (46%), followed by ascidians
(27%), hydroids (18%) and barnacles (9%). Taxa from
the ascidians, polychaetes and porifera are potentially
introduced and need further analysis to confirm their
identity. These species were detected in association
with wharf facings, floating docks, channel markers,
and as biofouling on international vessel hulls.
Fourteen percent of the species detected on international
vessel hulls were not detected in the port environs,
inferring that international vessels are a potential vector
of concern as they may transfer new species to the
region.
Historically, and in modern times, biofouling is
one of the primary mechanisms that introduced marine
species are transferred between locations (Godwin 2003;
Hewitt et al. 2004; Ashton et al. 2006; Davidson et al.
2008; Hopkins and Forrest 2008; Mineur et al. 2008;
Lee and Chown 2009; Galil et al. 2014). This vector
is relatively poorly managed (Hewitt and Campbell
2007; Lee and Chown 2009), although a number of
countries have introduced guidelines regarding vessel
management that specifically targets introduced
marine species vectoring via biofouling (e.g., USA:
California Hull Fouling Legislation Assembly Bill
740 (AB 740)). It’s not surprising that a lag period
for development and implementation of biofouling
management guidelines exists, given the 14-year lag
period we’ve seen for the adoption of the Inter-
national Convention for the Control and Management
of Ships Ballast Water and Sediments Ballast Water
Convention in 2004.
A number of species of concern, that can become
pests, or are known as pests elsewhere, were detected
(e.g., the hydroids Eudendrium carneum Clarke,
1882 and Thyroscyphus fruticosus (Esper, 1793), the
bryozoan Watersipora subtorquata (d’Orbigny, 1852),
and a tentative identification of the Caribbean barnacle
Chthamalus proteus Dando and Southward, 1980).
These species have the potential to impact on native
fauna and flora in Palau, due to their propensity to
heavily foul substrata. Both E. carneum and T.
fructicosus were previously known and are believed
to have been introduced with a floating bridge that
came from China in 1996 (Lambert 2002; Colin
2009). The method of introduction for the other
species is unknown but likely associated with vessel
biofouling given that Palau receives little international
ballast water but it does receive a large number of
recreational vessels (such as touring yachts).
Of concern is that some of the species detected
have the potential to become pest species and
damage tourist destinations. A similar situation has
already occurred in Palau, with the introduction of
the cnidarian, Aiptasia sp., into one of the major
international tourist destinations, Ongeim’l Tketau
(Jelly Fish Lake; Colin 2009), located on the rock
island of Mecherchar. Palau relies on the tourism
industry, with 11% of the gross domestic product
being tourist related (US Department of State 2012)
and thus impacts upon drawcard tourist destinations
could have serious implications for the country’s
economy.
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M.L. Campbell et al.
Table 4. Detected introduced, cryptogenic and potentially introduced species during the preliminary Palau introduced species survey.
Species are listed with an indication of the sampling locations/sites (wharves, moorings, vessel hulls, or “pristine” locations without
commercial activity). A “●” indicates presence upon a substrate. Please note that scientific names and taxonomic authorities (for species
names) were verified using the WoRMS database (http://www.marinespecies.org/).
Phyla
Species
Status
Porifera
Haliclona caerulea? (Hechtel, 1965)
Mycale sp. (orange sponge)
Eudendrium carneum Clarke, 1882
Obelia sp.
Thyroscyphus fruticosus (Esper, 1793)
Sabellastarte sp.
Serpulididae
Potential
Potential
Introduced
Cryptogenic
Introduced
Potential
Potential
Cryptogenic
(cosmopolitan)
Introduced
Introduced
Introduced
Introduced
Introduced
●
Hydroida
Polychaeta
Cirripedia
Bryozoa
Ascidia
Pisces
Amphibalanus amphitrite (Darwin, 1854)
Chthamalus proteus Dando and Southward, 1980
Amathia distans Busk, 1886
Virididentula dentata (Lamouroux, 1816)
Bugula neritina (Linnaeus, 1758)
Tricellaria occidentalis (Trask, 1857) /
T. inopinata D’Hondt and Occhipinti Ambrogi, 1985
Watersipora subtorquata (D’Orbigny, 1852)
Ascidia sydneiensis Stimpson, 1855
Botryllus sp. (cf. niger)
Didemnum perlucidum Monniot F., 1983
Phallusia nigra Savigny, 1816
Diplosoma listerianum (Milne Edwards, 1841)
Gobiidae sp.
Styela plicata (Lesueur, 1823), a species that is
native to Palau, but has been introduced to Australia
(e.g., Glasby 1999; Wyatt et al. 2005) and elsewhere
(e.g., da Rocha and Kremer 2005; de Barros et al.
2009), was detected in moderate densities at the
commercial wharves on facings. This species is a pest
in some regions (e.g., Glasby 1999), reaching high
densities and fouling infrastructure (e.g., Glasby 1999;
Connell 2000). Given the presence of this species in
the port environment, it is possible that Palau may
act as a donor region for this species, with a pathway
related to international recreational vessels that visit
Palau during larger treks.
Pre-existing literature
Previous introduced species and biodiversity research
from Palau (Lambert 2002; Golbuu et al. 2005;
Colin 2009), and the wider Indo-Pacific biogeographic
region including: tropical Australia (Hewitt 2002),
Guam (Paulay et al. 2002), Samoa and American
Samoa (P. Skelton, pers. comm.), had collectively
identified 127 introduced or cryptogenic marine or
estuarine taxa. Ascidians represent a substantial
portion (33%) of these introductions, followed by
bryozoans (11%), hydroids (11%) and then bivalves
(9%; Figure 2). Based on life-history characters and
358
Introduced
Potential
Potential
Introduced
Introduced
Introduced
Potential
Wharves
Vessels
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Mooring
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the timing of likely introduction, species were
assigned association with primary vectors of
introductions (e.g., ballast water, vessel biofouling,
intentional aquaculture species and hitch-hiker
aquaculture species). The majority of species (98%)
have traits that indicate vessel biofouling is the highest
likelihood vector, however the vectors of ballast
water (40%), aquaculture hitch-hikers (39%) and
intentional introductions (31%) have a substantial
proportion of species that may have been transported
by these means.
Within Palau, six introduced and 13 cryptogenic
species have been identified through biodiversity work
undertaken by the Coral Reef Research Foundation
(Lambert 2002; Colin 2009; supplementary material
Table S1). Within (Western) Samoa and American
Samoa, nine introduced species have been detected
(P. Skelton, pers. comm.; Table S1). Similarly, within
Guam 40 introduced and 45 cryptogenic species have
been detected by surveys using the Bishop Museum
protocols (Paulay et al. 2002; Table S1). Surveys
using the Hewitt and Martin protocols have detected
25 introduced species and six cryptogenic species
within tropical Australia (Hewitt 2002; Table S1).
Of the potential and possible introduced species
in Palau, there are no shared introduced and cryptogenic species with tropical Australia; however Palau
Taxa
Introduced marine species in Palau
Figure 2. Number of
introduced and cryptogenic
marine species by taxa
introduced into Palau,
Guam, Samoa and tropical
Australia.
Echinodermata
Arthropods ‐ isopoda
Arthropodes ‐ cirripedia
Molluscs ‐ gastropoda
Cnidaria ‐ anthozoa
Arthropods ‐ malacostrata
Algae
Porifera
Pisces
Polychaeta
Mollusca ‐ bivalvia
Cnidaria ‐ hydrozoa
Bryozoa
Urochordata
0
and Samoa share one introduced species (T. fruticosa),
and Palau and Guam, share three introduced species
(Didemnum perlucidum Monniot F., 1983, Diplosoma
listerianum (Milne Edwards, 1841), Lissoclinum fragile
(Van Name, 1902)). The lack of species-sharing between
regions may be an artefact of taxonomic effort, or
a result of the qualitative versus quantitative nature
of the survey sampling methods used in these areas.
Alternatively, this lack of overlap may also be due to
the dearth of pathways shared between the regions;
however this seems unlikely given that these regions
are historically linked by wartime activity during
WWII, and currently linked by recreational traffic
(Oliver 1989; Marti 2004) and in some instances
commercial traffic (Campbell and Hewitt 1999; Ruiz
et al. 2015). We note however, that commercial traffic
has been reduced with modernisation of ports and
vessels (e.g., Ward 1989).
Detecting and identifying introduced marine species
The combined literature review and preliminary
baseline survey identified a total of 11 introduced,
17 cryptogenic and 12 potentially introduced species
for Palau. These species were typically associated
with artificial substrates, such as wharves, floating
buoys and vessel hulls.
Recommendations
When this research was undertaken Palau had two
pieces of legislation relating to non-native species:
Palau National Code Title 25, Chapter 20 refers to
Quarantine laws; and in 2004 Palau published the
Palau National Invasive Species Strategy (https://www.
cbd.int/doc/submissions/ias/ias-pw-strategy-2007-en.pdf),
which included the establishment of The National
Invasive Species Committee (NISC). In 2006, the
5
10
15
20
25
30
35
40
45
50
Numbers
position of National Invasive Species Coordinator
was created and filled; this position also acts as the
secretary for the NISC. In March 2016, the Palau
President signed into law the Biosecurity Act
(http://www.paclii.org/pw/legis/num_act/ba2014rn9582015241/).
This new law contains an update to Quarantine laws
(http://www.islandtimes.us/index.php?option=com_content&vie
w=article&id=644:biosecurity-bill-becomes-law). Many aspects
of the early legislation is focussed or implemented in
an agricultural and land management context, with
an outward focus on preventing pest species
reaching Palau. After this initial training exercise (as
described in this paper), non-native marine species
and survey expertise was established and initiatives
were put in place to consider and improve the management of marine ecosystems. The Palau National Invasive
Species Committee is very pro-active and involved
in further initiatives across the Pacific island region
(http://www.palaunisc.org/news--noteworthy/archives/06-2016).
Based on dialogue during the workshop and
outcomes of the field survey, the following recommendations were made to the OERC and various
State Governments to improve introduced marine
species management in Palau:
1. An evaluation of the roles and responsibilities of
national and state governments for marine
biosecurity delivery needs to occur;
2. A full baseline port survey, including regions
beyond Koror State, should be implemented to
gauge the presence of introduced and cryptogenic
species that may cause high risk impacts to
economic, cultural, social and environmental
values. The preliminary findings suggest that
commercial and non-commercial vessel areas
(e.g., tourist destinations) are a high priority. We
note that since the initial sampling reported here,
359
M.L. Campbell et al.
3.
4.
5.
6.
7.
8.
additional sampling has started to occur and is
ongoing (I. Olkeriil, pers. comm.). However, the
recommendation that a full baseline port survey
be conducted has not been acted upon;
Risk assessments should occur to determine high
risk routes (pathways), and transport vectors into
Palau and into different Palau islands. By
understanding the pathways and vectors of introduced species effective management strategies
can be formulated;
A risk assessment of high risk species that pose a
future threat to Palau should be conducted to aid
in the creation of effective preparedness plans
that include targeted surveillance, with rapid
response plans (also see points 6 and 7);
A programme for inspection of high risk vessels
(based on risk assessments) entering Koror State
should be considered. Consideration of domestic
borders and pathways should also occur;
An action plan that details how the detection of
an introduced species should be dealt with and
delineates the government agencies that are
responsible for different tasks within the action
plan should be developed;
Eradication and management plans for a number
of potential high risk species should be
developed for rapid implementation in the
likelihood that a high risk introduced species is
detected; and
Mooring buoys and ropes at tourist destinations
need to be changed frequently to prevent the
transfer and establishment of introduced species
between tourist locations.
For a number of reasons, including limited resources,
most of these recommendations have had no, or only
partial, implementation. Palau continues to explore
avenues for obtaining resources for this purpose.
It should be noted that a Regional Biosecurity
Plan (RBP) for Micronesia and Hawaii has been
developed and adopted in association with build-up
of US Government resources in Guam. The assessment
for the RBP evaluated both direct and regional risks
and impacts across terrestrial, freshwater and marine
systems and included several elements of the
recommendations listed above in the marine assessment (Ruiz et al. 2015) The Strategic Implementation
Plan (SIP) for the RBP outlines numerous activities
for implementation of the plan; activities specific to
Palau include a number of marine-related activities,
including development and adoption of hull fouling
regulations, and building capacity to enforce such
regulations.
360
Conclusions
Palau is a pristine destination that attracts a large
number of international tourists; however introduced
marine species are becoming prevalent in this region,
which could have economic implications for tourism.
The Palau government is pro-actively attempting to
prepare for the impacts that may be associated with
introduced species. As part of this preparation, an
introduced marine species capacity building exercise
that combined both theory and field experience was
implemented within Koror State. This was managed
via a workshop that trained 10 Palau and two
international agencies in introduced marine species
and port survey techniques. The survey and subsequent
literature review detected 11 introduced, two cryptogenic and seven potentially introduced species. A
series of recommendations were made to aid Palau
in its ability to prepare and deal with introduced
marine species. This work is preliminary in nature
and continued efforts on introduced species management are needed to ensure Palau is fully prepared for
this global problem of introduced marine species.
Acknowledgements
This work was partially funded by the IUCN, TOTAL, the Marine
Biosecurity Education Consortium (funded by the Australian
Department of Environment), and the Australian Maritime
College. The Palau Office of Environmental Response and
Coordination and the Koror State Government provided funding
for extending the field survey and undertaking species
identification. We wish to acknowledge and thank the people that
took part in the training and provided information, particularly
Ilebrang Okeriil (regulatory and implementation information), and
Lori and Patrick Colin of the Coral Reef Research Foundation
(CRRF). Lori and Patrick strongly advocated for capacity
building in Palau that led to this work and provided substantive
pre-existing taxonomic information and identifications as part of
the US National Cancer Institute Marine Natural Products
Collection program. We also thank and acknowledge Carmen
Primo (University of Tasmania) for identification of ascidian
samples. Last, we thank and acknowledge the reviewers for their
constructive comments.
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Supplementary material
The following supplementary material is available for this article:
Table S1. Pre-existing knowledge of introduced and cryptogenic species in Palau, Guam, Western and American Samoa, and tropical Australia.
Appendix 1. Taxonomic databases and networks (listed alphabetically).
Appendix 2. Taxonomic bibliography.
This material is available as part of online article from:
http://www.reabic.net/journals/mbi/2016/Supplements/MBI_2016_Campbell_etal_Supplement.xls
http://www.reabic.net/journals/mbi/2016/Supplements/MBI_2016_Campbell_etal_Appendix1.pdf
http://www.reabic.net/journals/mbi/2016/Supplements/MBI_2016_Campbell_etal_Appendix2.pdf
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