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AQUACULTURE ENVIRONMENT INTERACTIONSAquacult Environ
Interact
Vol. 7: 147166, 2015doi: 10.3354/aei00138
Published online September 17
INTRODUCTION
Shell middens dating to as early as 12 000 BC inEurope, America,
Japan, Australia and South Africaindicate that molluscs have been
harvested exten-sively for millennia (e.g. Bailey & Milner
2002, Og -burn et al. 2007, Erlandson et al. 2008, Haupt et
al.2010, Habu et al. 2011). Oysters were highly re -
garded by the classical Romans who imported oys-ters from as far
away as Britain, despite the proposalof a law in 115 BC to curb
this practice (Andrews1948). This demand undoubtedly prompted
attemptsat culturing oysters and resulted in the
successfulestablishment of oyster beds in a lake off thegreater Bay
of Naples in 105 BC (Andrews 1948). Atabout the same time,
Aboriginal Australians were
The authors 2015. Open Access under Creative Commons
byAttribution Licence. Use, distribution and reproduction are un
-restricted. Authors and original publication must be
credited.Publisher: Inter-Research www.int-res.com
*Corresponding author: [email protected]
REVIEW
Polydorid polychaetes on farmed molluscs: distribution, spread
and factors contributing
to their success
C. A. Simon1,*, W. Sato-Okoshi2
1Department of Botany and Zoology, Stellenbosch University,
Matieland Private Bag X1, Stellenbosch, South Africa2Laboratory of
Biological Oceanography, Graduate School of Agricultural Science,
Tohoku University, Sendai 981-8555, Japan
ABSTRACT: Species of the Polydora-complex (i.e. polydorids) are
the most common shell-boringpolychaetes found on cultured molluscs.
However, which species become problematic depend ontheir ability to
reach mollusc farms and flourish under culture conditions. We
therefore hypo -thesise that the planktonic larval phases of pest
polydorids on molluscs grown on-shore will beshort (as is typical
of adelphophagic larvae, which can maintain large local
populations) whilethose of polydorids on molluscs grown off-shore
will be long (as is typical of planktotrophic larvae,which can
disperse long distances to farms). Principal component and
discriminant analyses ofinformation extracted from the literature
partly supported this hypothesis by identifying larvaldevelopmental
mode and pest species as contributing more to pest status than host
species andculture mode, with differential influence on pest status
in different situations and potential biasthrough incorrect
identification of polydorid species. 2 analyses confirmed that pest
statusdepended on host culture method and pest larval mode. Pest
polydorids producing adelphophagiclarvae in on-shore systems may
reflect the development of large local populations on hosts
withculture periods >2 yr. The many records of pests in
off-shore and near-shore systems with pestspecies producing
planktotrophic larvae may reflect shorter host culture periods and
the higherincidence of planktotrophy among polydorid species in
general. Polydora websteri, P. uncinata, P.hoplura and P. haswelli
are the most frequently recorded and widespread pest species
globally,although the taxonomy of these and shell-boring P. ciliata
and Boccardia polybranchia need to beclarified. The positive
relationships between the numbers of alien shell-borers and pests,
and thenumber of hosts cultured per country confirm that mollusc
aquaculture is an important vector andreservoir of alien pest
polychaetes.
KEY WORDS: Alien species Aquaculture Larval developmental modes
Molluscs Off-shore On-shore Polydorid pests
OPENPEN ACCESSCCESS
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Aquacult Environ Interact 7: 147166, 2015148
farming oysters by catching spat on cultch (Ogburnet al. 2007).
The continued demand for oysters andother molluscs has led to the
overexploitation of nat-ural stocks and consequent attempts to
replenish de - pleted stocks with animals imported from
elsewhereand the establishment of culture systems (e.g. Wolff&
Reise 2002, Ruesink et al. 2005, Og burn et al. 2007,Haydar &
Wolff 2011, Castell 2012, Lucas 2012). InJapan, China and Korea the
culture of molluscsbegan about 500 yr ago (Kusuki 1991 in Ruesink
etal. 2005) while in Europe and North America itstarted in earnest
in the 1700s and 1800s (Wolff &Reise 2002).
Modern culture of molluscs is often associated withlarge-scale
movement of stock (Wolff & Reise 2002,Ruesink et al. 2005,
McKindsey et al. 2007). At least 5species of oysters and 2 species
of clams have beenimported to, and moved among, countries in
westernand northern Europe for aquaculture purposes sinceas early
as 1570 (Wolff & Reise 2002). On the westcoast of North
America, most of the cultured speciesare exotic or alien (McKindsey
et al. 2007) while inChile a thriving abalone industry relies on
stock orig-inally imported from California and Japan (Morenoet al.
2006). Similarly, the South African oyster indus-try relies on the
regular importation of spat from theAmericas and Europe and the
local movement ofstock from nursery to grow-out facilities (Haupt
etal. 2010, 2012). Up to 18 oyster species have beentranslocated to
73 countries or regions, with the Paci -fic oyster, Crassostrea
gigas, translocated to morethan 50 (Ruesink et al. 2005, Lucas
2012). Gastropodsare moved less frequently and there is a tendency
forindigenous species to be cultured (Castell 2012, butsee Culver
et al. 1997 and Moreno et al. 2006).
The cultivation of high densities of molluscs canhave
far-reaching ecological effects, creating habi-tats for other
organisms, providing them with pro-tection against predators,
reducing physical andphysiological stress and enhancing settlement
andre cruitment (e.g. Pregenzer 1983, Ruesink et al.2005, McKindsey
et al. 2007, Lucas 2012). This isparticularly important when the
molluscs are cul-tured in environments where they are creating
hardsubstrates where none existed before, such as inmuddy or
soft-sediment environments and sus-pended culture (Ruesink et al.
2005, McKindsey etal. 2007), thus providing settlement substrates
forlarvae that might have been otherwise lost. Thearrangement of
the molluscs and their shell struc-ture may further contribute to
the production of dif-ferent microclimates for preferential
settlement bylarvae; for example, large numbers of planktonic
polydorid larvae settled in the inner, rather thanouter, valve
of scallops in suspended culture inJapan (Teramoto et al. 2013).
Thus, cultured mol-luscs are often associated with infestations by
dis-ease agents and fouling organisms (e.g. Bower et al.1994, Wolff
& Reise 2002, McKindsey et al. 2007,Haydar & Wolff 2011,
Castell 2012, Lucas 2012).This, together with the extensive
movement of mol-luscs, particularly of oysters, has led to
aquaculturebeing considered one of the main vectors of trans-port
of exotic species. For example, Wolff & Reise(2002) estimated
that more than 20 species of ani-mals were imported to Europe with
C. gigas alone,and they concluded that oysters are more
importantvectors than either hull fouling or ballast water,
aconclusion supported by McKindsey et al. (2007).
There are many reviews of the diseases of cul-tured molluscs and
of the exotic species transportedwith these animals, but they
seldom focus on shell-boring polychaetes in any detail (Bower et
al. 1994,Mor ten sen et al. 2000). The most common shell-borers are
members of the Polydora-complex, oftenre ferred to as polydorids
(e.g. Blake 1969b, Morenoet al. 2006, Radashevsky et al. 2006,
Sato-Okoshi etal. 2008, Boon zaaier et al. 2014). While there
arerare in stances where high infestations by polydoridsoccur under
natural conditions (e.g. Poly do ra bre-vipalpa in the scallop
Patino pecten yesso ensis andPolydora uncinata in the oyster Crasso
strea gi gas[Sato-Okoshi & Abe 2012], and Di poly dora con
-vexa, D. con cha rum and D. alborectalis in the scal-lop Patino
pecten yessoensis in Japan [Sato-Okoshi1999]), high in festation by
a few polydorid speciesis observed more frequently in mollusc
culture sys-tems where intensive commercial culture may leadto the
development of ecosystems which may en -courage the proliferation
of pests. For example, inSouth Africa, Chile and Australasia,
farmed mol-luscs were typically infested by fewer species thanare
present on wild molluscs occurring close tofarms (e.g. Sato-Okoshi
& Takatsuka 2001, Simonet al. 2006, Sato-Okoshi et al. 2008,
Simon et al.2010, Simon 2011, Boonzaaier et al. 2014, Sato-Okoshi
et al. 2015). Similarly, molluscs grown inon-shore culture systems
were infested by fewerspecies than those grown off-shore (Simon,
2015).This suggests that either only some species areprone to
becoming pests in culture, or that the cul-ture environment creates
favourable conditionswhich only enable some species to become
pests.In cases of high infestation levels, shells are dam-aged by
the boring activity of the worms whichnegatively impact condition
in the hosts as they
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Simon & Sato-Okoshi: Polydorid polychaete pests on cultured
molluscs
divert energy from growth to shell repair (Kojima &Imajima
1982, Lleonart et al. 2003, Simon et al.2006). In extreme cases
infestation has been impli-cated in causing high mortalities (for
ex ample, upto 50% of abalone stock in Tasmania, Lleonart etal.
2003) and the collapse of oyster culture con cernsin Hawaii and
Australia (e.g. Bailey-Brock 1990,Ogburn et al. 2007).
The main aim of this review was 2-fold. In the firstinstance,
the literature was explored to determinewhether pest species,
larval developmental mode,host species and culture method influence
the peststatus of polydorids on cultured molluscs. The secondaim
was to provide the first review of polydorid pestson cultured
molluscs on a global scale. Such a reviewwill help to (1) highlight
which species are mostproblematic globally, (2) alert importers of
molluscsto the species that are problematic in the countriesfrom
which their molluscs originate, (3) trace the pos-sible source of
new alien pest species, (4) determineif any species show host
specificity and (5) highlightproblems in species
identification.
MATERIALS AND METHODS
Reviewing the literature
A review of the literature reporting shell-infestingpolydorids
in cultured or commercially harvestedmolluscs was conducted and the
following informa-tion extracted: location, the polydorid and host
spe-cies, culture method (classified as on-shore, inter-tidal,
near-shore [bottom and subtidal] and off-shoresuspended), pest
status (rare, common and pest) andlarval developmental mode
(planktotrophic, adel -pho phagic, lecithotrophic and
poecilogonous). Aspecies was classified as pest, when it was called
assuch by the author, when the author demonstrated asignificant
negative impact on the host or wheninfestation exceeded 10 worms
per individual (seeKojima & Imajima 1982). It was classified as
com-mon if many of the hosts were infested, but theauthor did not
consider it a pest or had not demon-strated a negative impact on
the host (this usuallyapplied to small species which were often
present inhigh densities without negatively affecting the host,or
if the boring activity of the worm was not destruc-tive), or if the
infestation level was 0.9. These were run through a descriptive
dis-criminant analysis (DA) to detect differences in peststatus
depending on host, culture method, pest spe-cies and larval
developmental mode.
A 2 analysis was used to test the hypothesis thatthe larval
development of pests depends on the cul-ture system in which the
molluscs are reared, usingonly those records from the literature
which indi-cated both the pest status and larval developmentalmode
of the polydorids in question, and previouslyunpublished data
collected by the authors.
Simple linear regressions were used to determinewhether there
was a relationship between the num-ber of hosts cultured and the
number of shell-infesting, non-indigenous polydorids and
non-indigenous pest polydorids recorded per country,and between the
number of shell-boring, non-indige-nous polydorid species and the
number of shell-bor-ing, non-indigenous pest polydorids re corded
oncommercially reared hosts, per country. For the latterana lysis,
cryptogenic species, species which had onlybeen identified to genus
level and references to P. cil-iata (this species is not a
shell-borer and will be dis-cussed in more detail in Problems with
taxonomybelow) were omitted as their alien statuses could notbe
confirmed.
149
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Aquacult Environ Interact 7: 147166, 2015150
WHY DO ONLY SOME POLYDORID SPECIESBECOME PESTS?
Culture methods
Molluscs are cultured in a variety of ways whichdiffer in terms
of location, production costs, feedingand exposure of the molluscs
to water movement andair (Appleford et al. 2012, Castell 2012,
Lucas 2012).In on-shore systems, animals may be grown in bas-kets,
cages or bags suspended in outdoor raceways,ponds or dams, or
indoor tanks; water is usuallypumped in from the sea, through the
farm and backto sea, while the molluscs are usually constantly
sub-merged (Appleford et al. 2012). Alternatively, ani-mals may be
grown in on-bottom culture where spator hatchery-reared seed are
sowed directly onto theseabed or suspended off long-lines or
floating rafts incages or bags subtidally or in the off-shore
(Nell2001, Appleford et al. 2012, Castell 2012, Lucas2012). These
will also be submerged permanently,but are subject to prevailing
water currents whichwill depend on depth and distance from the
shore.These systems can be utilised for most molluscs. Cer-tain
bivalves may also be grown in the intertidal; spatare captured on
sticks, nets or in bags which are seton frames or trestles or they
may be sowed directlyonto the rocks (Nell 2001, Appleford et al.
2012,Lucas 2012). These animals are exposed during lowtide. Animals
in near- and off-shore and intertidalculture are seldom fed. Thus,
depending on the cul-ture method, molluscs will experience
different lev-els of water movement and exposure during tidalcycles
which could, in turn, influence their exposureto larvae of fouling
organisms. Additionally, thedegree of feeding of the molluscs may
influence theamount of food available to shell-boring worms,which
could further affect their populations.
Larval developmental modes
The success of shell-boring pest polychaetes canprobably be
attributed to favourable conditions onfarms relative to the natural
environment. Simon etal. (2005) suggested that the enhanced
reproductiveoutput and recruitment of the pest sabellid poly-chaete
Terebrasabella heterouncinata could proba-bly be attributed to the
high availability of potentialhosts and suspended organic matter
derived fromdegraded abalone food and faeces, which may havebeen
further influenced by the nature of the abalonefeed (Simon et al.
2002). Similarly, the high volumes
of faeces and pseudofaeces produced by culturedbivalves (Lucas
2012) may also contribute to the suc-cess of pest polychaetes.
Furthermore, the success ofpests may be related to their life
history strategies;polydorids usually have high fecundity, with
somespecies producing >5000 planktotrophic larvae perbrood, and
an average of approx. 2574 (Blake 1969a,Sato-Okoshi et al. 1990,
Blake & Arnofsky 1999)which may result in high propagule
pressure. How-ever, not all worms that become established on
farmsbecome pests (e.g. Dipolydora capensis on farmedabalone in
South Africa) (Simon et al. 2006, Simon &Booth 2007, Boonzaaier
et al. 2014, Simon 2015). Thediscrepancies between the shell-boring
polydoridworms that could be im ported onto mollusc farmsand those
that do become established, and betweenthe degrees to which the
different species flourish,may be related to differences in the
larval develop-mental modes among polydorids (Simon 2015).
Polydorids lay their eggs in capsules brooded in thematernal
burrows, but species differ with respect tothe size, number and
feeding mode of larvae pro-duced; females may produce many
planktotrophiclarvae, few adelphophagic larvae which feed on
un-fertilised nurse eggs in the brood capsules, or
fewlecithotrophic larvae which are nourished by endo -genous yolk
(Gibson 1997, Blake & Arnofsky 1999,Blake 2006). Planktotrophic
larvae usually emergefrom the maternal burrow when 3 to 8
chaetigerslong, while adelphophagic and lecitho trophic
larvaeemerge when 5 to 19 chaetigers long (Blake 1969a,Blake &
Arnofsky 1999). Some species are poecilogo-nous, thus producing
different types of larvae as de-scribed above, either by the same
individual, or dif-ferent individuals within the same population
(Gibson1997, Blake & Arnofsky 1999, Blake 2006, David et
al.2014). However, irrespective of the size at emergencefrom the
maternal burrow, the larvae of most speciesmetamorphose when they
are 15 to 20 chaetigers and900 to 1600 m long (Blake & Arnofsky
1999, David &Simon 2014). This also coincides with the size
atwhich larvae usually become too heavy to swim ac-tively and sink
in preparation for settlement (Hansenet al. 2010). Thus, the time
spent in the water columndepends on the difference between the size
at emer-gence and the size at metamorphosis; depending onwater
temperature, planktotrophic larvae can spendup to 85 d in the water
column before settling, whilelarger adelphophagic or lecithotrophic
larvae can set-tle within a day of emergence (Blake &
Arnofsky1999). Thus the larval developmental modes of spe-cies will
ultimately affect the ability of their larvae toreach molluscs in
culture.
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Simon & Sato-Okoshi: Polydorid polychaete pests on cultured
molluscs
Predictions
We hypothesised that species which become pestsdepend on their
larval developmental modes and theculture methods applied to the
hosts for 3 reasons: (1)molluscs farmed in off-shore and on-shore
conditionsare exposed to different levels of sea water move-ment,
(2) the duration of the planktonic phases of dif-ferent polydorid
species differ and (3) competent lar-vae are of a similar size. In
on-shore culture systems,larvae produced in wild source populations
mayenter farms with water pumped onto the farm, but,irrespective of
the duration of their planktonicphases, only competent larvae can
infest the mol-luscs and remain in the system. If the adult
wormsthen produce larvae with an obligate protractedplanktonic
phase, these will be lost from the systemvia the outflow. Thus
resident worms will probablynot contribute to the establishment of
large local pop-ulations on farms and we can predict that worms
withthis life history strategy will not become very abun-dant in
on-shore systems. By contrast, if the larvalplanktonic phase is
short or absent, resident wormswould contribute to the
establishment of a large localpopulation as the larvae remain on
the farm, infest-ing the same or nearby hosts (David et al. 2014,
seealso Simon 2005 concerning T. heterouncinata). Wecan therefore
predict that species producing larvaethat emerge at a very late
stage of development willdominate in on-shore culture systems.
In near-shore or off-shore culture systems, molluscswill be
exposed to the prevailing currents and plank-ton which can include
high densities of spionid(including polydorid) larvae (e.g.
Omelyanenko &Kulikova 2002, Abe et al. 2014). The plankton
willpresumably include larvae that may have long orshort planktonic
phases, but probably more of theformer; of the larvae captured
off-shore in OnagawaBay by Abe et al. (2014), 3 of the 5 spionids
identifiedto species level are known to produce
planktotrophiclarvae (Blake & Arnofsky 1999, Teramoto et al.
2013),while Polydora uncinata, a species known to producelarvae
with short planktonic phases and found wildin this bay (Sato-Okoshi
& Abe 2012) were absent.Thus we can predict that in off-shore
and near-shorecultures molluscs will be infested primarily by
spe-cies producing larvae with long planktonic phases.However, if
species which produce lecithotrophic oradelphophagic larvae are
introduced to off-shoreculture systems by way of infested molluscs,
then wecan expect these worms to remain on these farms andflourish
(for example, it has been suggested that thesudden appearance of P.
uncinata in oysters in sus-
pended culture in South Korea was a consequence ofthe
introduction of new oyster stocks from a differentsource population
[Sekino et al. 2003, Sato-Okoshi etal. 2012]).
Results and discussion
Influence of pest species and larval developmentalmode, and host
species and culture method
on pest status
Eightyinstancesofinfestation(fromtheliteratureandunpublished
data collected by the authors of thepresent study) included
informationof the larvaldevel-opmental modes of the pest and the
culture method ofthe hosts (the pest and host species in cluded in
thisanalysis are in bold in Table 1). These records included23
species of poly dorids infesting 19 host species(Table 1). Ap
proximately half of the records werefrom off-shore culture systems,
a third from on-shoresystems, a quarter from near-shore systems and
only5% from intertidal culture systems (Table 2). Further-more,
when all the records are considered (i.e. not justthose included in
the PCA analysis), we found thatmost species (14) were in off-shore
culture systems, 9in on-shore, 8 in near-shore and 3 in the
intertidal.
The PCA extracted 4 components but only 2 hadeigenvalues >0.9
which explained a total of 62.45%of the variation in the sample.
Discriminant analysesof these components showed that the model
wasvalid (Boxs M = 6.65, p > 0.05) and that component 1(larval
developmental mode and polychaete species)explained 92.6% of the
variance in pest status. Withthe exception of P. hoplura and P.
websteri, the poly-dorid species considered here only ever
producedone type of larva in all records (different develop-mental
modes were also recorded for Boccardiachilensis, which was not
included in the analysis,Table 1). Thus larval developmental mode
and poly-dorid species may to a large extent be surrogates ofeach
other. Furthermore, 22% of the species (P. ona-gawaensis, P.
uncinata, P. has welli, P. websteri and P.hoplura) accounted for
58% of the records. However,this analysis cannot account for
species which mayhave been misidentified; consequently the
impor-tance of pest species may have been overestimated.Component 2
(host and culture method) contributed
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Aquacult Environ Interact 7: 147166, 2015152
Species name Type region Country where Host infested present on
cultured molluscs
Boccardia
B. acus New Zealand New Zealand Crassostrea gigas, Tiostrea
chilensis
B. atokouica New Zealand New Zealand C. gigas
B. chilensis Chile Australia, New Zealand C. gigas, Mytilus
edulis, Saccostrea cucullata, T. chilensis
B. knoxi New Zealand Australia, New Zealand C. gigas, Haliotis
rubra
B. polybranchia Australia Australia, France C. gigas, M.
edulis
B. proboscidea West coast of USA Australia, Japan, C. gigas,
Haliotis midae South Africa, USA (Hawai)
B. pseudonatrix South Africa Australia, South Africa C. gigas,
Saccostrea commercialis, H. midae
B. semibranchiata France (Mediterranean) France, Spain C.
gigas
BoccardiellaB. hamata East coast of USA China, Japan C. gigas,
pearl mussels
Dipolydora D. alborectalis Sea of Japan, Vostock Bay Japan
Patinopecten yessoensis
D. armata Atlantic Ocean, Madeira Japan, South Africa Haliotis
discus hannai, Haliotis diversicolor, H. midae
D. bidentata Sea of Japan, Japan C. gigas, P. yessoensis Peter
the Great Bay
D. capensis South Africa South Africa H. midae
D. cf. giardi South Africa South Africa H. midae
D. concharum New England to Japan P. yessoensis Newfoundland
D. giardi Spain Chile, Japan Argopecten purpuratus, C. gigas,
Ostrea chilensis
D. huelma Chile Chile Haliotis rufescens
D. keulderae South Africa South Africa C. gigas, H. midae
D. normalis South Africa South Africa H. midae
D. socialis Pacific Ocean, Chile Chile O. chilensis
PolydoraP. aura Japan Japan, Korea C. gigas, H. discus discus,
Pinctada fucata
Table 1. Global distribution of shell-infesting and pest species
that are associated with cultured or commercially harvested
mol-luscs. Excludes species identified just to genus level. Pest
status in native and invasive range given as pest (p), common (c),
or rare(r). Larval developmental mode: adelphophagy (ad),
lecithotrophy (le), planktotrophy (pl), poecilogony (po). Culture
environment:
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Simon & Sato-Okoshi: Polydorid polychaete pests on cultured
molluscs 153
Pest status Pest status No. of pest Larval Culture Reference in
native outside of records developmental environ- range native range
(total records) mode ment
p 1(3) po int, off-s, nr Handley (1995), Handley & Bergquist
(1997), Dunphy et al. (2005)
c 0(1) ? off-s Handley (1995)
p & c 1(6) ad, pl int, off-s, Skeel (1979), Pregenzer
(1983), Handley (1995), nr Handley & Bergquist (1997), Nell
(2001), Dunphy et al.
(2005)
p p 4(4) pl off-s, nr Handley (1995), (2000), Lleonart (2001),
Nell (2001),Lleonart et al. (2003)
c p 1(2) ? int, off-s Pregenzer (1983), Ruellet (2004), Royer et
al. (2006)
p, c, r 5(8) po int, on-p Bailey-Brock (2000), Sato-Okoshi
(2000), Simon et al. (2006), Simon & Booth (2007), Simon et al.
(2010), Walker (2014)
c, p r? 1(6) ad off-s, on-p Sato-Okoshi et al. (2008) (as
Boccardia knoxi), Simon etal. (2010), Sato-Okoshi & Abe (2012),
Walker (2014),Simon (2015), S. De Lange, C.A. Simon & L.G.
Williamsunpubl. data
r 0(2) ? int Ruellet (2004), Martinez et al. (2006), Royer et
al. (2006)
c 0(2) pl off-s Sato-Okoshi (2000), Zhou et al. (2010)
p 2(2) pl off-s Mori et al. (1985), Sato-Okoshi (1999)
p 1(2) ? on-p Simon (2011), W. Sato-Okoshi unpubl. data
p c 1(2) pl off-s, nr Sato-Okoshi (1999), W. Sato-Okoshi unpubl.
data
c 0(1) pl on-p Simon et al. (2006), Boonzaaier et al. (2014)
r 0(1) ? on-p Boonzaaier et al. (2014)
c 2(2) pl nr Mori et al. (1985), Sato-Okoshi (1999)
c 0(4) pl off-s Sato-Okoshi (1999), Sato-Okoshi & Takatsuka
(2001)
p 1(1) ? nr Vargas et al. (2005)
r 0(2) ? off-s, on-p Simon (2011), Boonzaaier et al. (2014)
r 0(1) ? on-p Simon (2011)
r 0(1) ? off-s Sato-Okoshi & Takatsuka (2001)
p 4(4) pl off-s, on-p Sato-Okoshi & Abe (2012), Sato-Okoshi
et al. (2012)
intertidal (int), near-shore bottom and subtidal (nr), off-shore
suspended (off-s), on-shore pond or tank (on-p). Pest status
columns:pest status is only in relation to the infestation of
cultured or harvested molluscs; blank spaces indicate that pest
status is not
known. ?: unknown. Species names in bold were included in the
principal component analysis
(continued on next page)
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Aquacult Environ Interact 7: 147166, 2015154
Species name Type region Country where Host infested present on
cultured molluscs
P. bioccipitalis California Chile Mesodesma donacium
P. brevipalpa Sea of Japan, Vostock Bay China, Japan H. discus
hannai, P. yessoensis
Brazil Brazil C. gigas, Crassostrea rhizophorae
P. ciliata England India, France, Germany, C. gigas, M. edulis,
Ostrea madrasensis, P. fucata, Italy, UK Tapes philippinarum
P. cornuta East coast of USA USA Crassotrea virginica
P. curiosa Pacific Ocean, Japan P. yessoensis Kurile Islands
P. ecuadoriana Ecuador Brazil C. gigas, C. rhizophorae
P. cf. haswelli Australia? Brazil C. gigas, C. rhizophorae
P. haswelli Australia Australia, Korea, Japan, C. gigas, M.
edulis, O. chilensis, New Zealand Pecten novaezelandiae, Perna
canaliculus, P. fucata, S. cucullata, H. discus discus
P. hoplura Bay of Naples Australia, Belgium, France, C. gigas,
M. edulis, H. midae, Haliotis Holland,New Zealand, tuberculata
coccinea, H. rubra, South Africa, Spain Haliotis laevigata (Canary
Islands)
P. onagawaensis Japan China, Japan C. gigas, Chlamys farreri, P.
yessoensis, H. discus hannai
P. rickettsi Southern California Argentina, Brazil, Chile
Aequipecten tehuelchus, A. purpuratus, Nodipecten nodosus, C.
gigas, H. rufescens
P. uncinata Japan Australia, Chile, Japan, C. gigas, H. discus
discus, H. discus hannai, Korea H. diversicolor, Haliotis
diversicolor supertexta, Haliotis gigantea, Haliotis roei, H.
laevigata
P. websteria East coast of USA Australia, Brazil, Canada, C.
gigas, C. rhizophorae, C. virginica, M. edulis, China, Japan,
Namibia, P. yessoensis, Placopecten magellanicus, P. fucata,
Mexico, New Zealand, Pinctada imbricata, S. commercialis, South
Africa, USA, S. cucullata, Saccostrea glomerata? Ukraine,
Venezuela
PseudopolydoraPs. dayii South Africa South Africa H. midae
Table 1 (continued)
aPreliminary data from Williams (2015) suggest that specimens
identified as Polydora websteri in southern Africa, Japan
andAustralia are molecularly distinct from specimens from the east
coast of America, and he consequently referred to them as
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Simon & Sato-Okoshi: Polydorid polychaete pests on cultured
molluscs 155
Pest status Pest status No. of pest Larval Culture Reference in
native outside of records developmental environ- range native range
(total records) mode ment
p 1(1) ? nr Riascos et al. (2008)
p 7(7) pl nr, off-s Imajima & Sato (1984), Sato-Okoshi
(1999),Sato-Okoshi & Abe (2012), Sato-Okoshi et al.
(2013),Teramoto et al. (2013)
r 0(2) le int Radashevsky et al. (2006)
p, r p 5(7) ? int, off-s Kent (1979), Velayudhan (1983), Ghode
& Kripa (2001), Boscolo (2002), Ruellet (2004), Buck et al.
(2005), Royer et al. (2006), Brenner et al. (2009)
p 1(2) ? int Gaine (2012) (as P. ligni)
r 0(1) le off-s Sato-Okoshi (1999)
p 1(2) pl int Radashevsky et al. (2006)
? ? ?(2) pl ?, int Radashevsky et al. (2006)
c p, c, ? 8(13) pl, ? off-s, int, Skeel (1979), Pregenzer
(1983), Read & nr, on-p Handley (2004), Read (2010),
Sato-Okoshi et al. (2012), Walker (2014), Sato-Okoshi & Abe
(2013)
p p, c, r, ? 11(20) ad, ad & pl int, off-s, Korringa (1951)
in Wolff & Reise (2002), Skeel (1979), on-p Pregenzer (1983),
Handley (1995), Lleonart (2001), Nell (2001), Lleonart et al.
(2003), Ruellet (2004), Royer et al. (2006), Simon et al. (2006),
Kerckhof et al.
(2007), Simon & Booth (2007), Bilbaa et al.
(2011),Boonzaaier et al. (2014), Walker (2014), Simon (2015),S. De
Lange, C.A. Simon & L.G. Williams unpubl. data
p 6(6) pl off-s Sato-Okoshi et al. (2013), Teramoto et al.
(2013), Williams (2015)
p 6(7) pl nr, off-s Sato-Okoshi & Takatsuka (2001),
Radashevsky & Cderas (2004), Vargas et al. (2005), Diez et al.
(2013)
p p 16(15) ad off-s Sato-Okoshi (1999), Radashevsky &
Olivares (2005), Sato-Okoshi et al. (2008, 2012), Sato-Okoshi &
Abe (2012), W. Sato-Okoshi unpubl. data
c, p c, p, r 12(26) ad, po, pl, ? int Loosanoff & Engle
(1943), Hartman (1954), Skeel (1979), Bailey-Brock & Ringwood
(1982), Bergman et al. (1982), Pregenzer (1983), Sato-Okoshi &
Nomura (1990), Bower et al. (1992), Handley (1995), Handley &
Bergquist (1997), Sato-
Okoshi (1999), Nell (2001), Diaz & Liero Arana (2003),Sabry
& Magalhes (2005), Sato-Okoshi et al. (2008,2013), Litisitskaya
et al. (2010) in Surugiu (2012), Read(2010), Simon (2011) (as P.
ciliata), Sato-Okoshi & Abe(2013), Simon (2015), Williams
(2015), De Lange et al.(2011), authors unpubl. data
r 0(1) pl on-p Simon et al. (2009)
Table 1 (continued)
P. cf. websteri. However, since this separation has not been
clarified, we here refer to all as P. websteri
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Aquacult Environ Interact 7: 147166, 2015
the records of C. gigas were from off-shore culturesystems, 6
were on-shore, and 2 were from the inter-tidal. For Patino pecten
yessoensis, 8 records eachwere from near-shore and off-shore
culture systems.Furthermore, Haliotis discus discus and H.
midaewere cultured in the same way in 4 out of 5 and 5 outof 6
records, respectively. Seven species wererecorded 2 or more times
and were always culturedin the same way. The importance of host
species andculture method is also highlighted when the inci-dence
of pests were considered for the most fre-quently recorded species.
In all of the records ofPatinopexten yessoensis in the near-shore
and 71%of the records in the off-shore, the polydorids
wereconsidered pests. Similarly, 71, 67 and 50% of the re -cords of
polydorids infesting C. gigas in the off-shore,on-shore and
intertidal, respectively, were of pests.
Although the PCA and discriminant analyses iden-tified 2
components which described the variability,the Wilks lambda values
were not statistically signif-icant (Wald = 0.951, 2(4) = 3.84, p =
0.428; Fig. 1). Thisindicates that polydorid species, culture
system, lar-val developmental mode and host species all con-tribute
to pest status, irrespective of the actual peststatus but that
different variables were important fordetermining the pest status
under different condi-tions. This was further explored using only
the re -cords of pests (which made up 79% of the records),with 2
analyses showing that the frequency of theinstances of pests
depended on mollusc culture system and the larval development of
the worms(2(6,55) = 30.12, p
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Simon & Sato-Okoshi: Polydorid polychaete pests on cultured
molluscs 157
maternal burrows coupled with their high survival,even if the
number of larvae per brood is low(Simon 2005, David & Simon
2014). Since relativelyfew adelphophagic larvae are produced per
broodand since they usually emerge just before theysettle (e.g.
Blake & Kudenov 1981, Gibson 1997,Blake & Arnofsky 1999,
Blake 2006) at a size whentheir swimming or dispersal ability is
reduced(Hansen et al. 2010), their ability to reach
off-shoreculture systems in appreciable numbers wouldprobably be
hampered. In spite of this, P. hopluraand P. uncinata, for which
only adelphophagy hasbeen widely recorded (e.g. Wilson 1928, Read
1975,Lleonart 2001, Sato-Okoshi 1998, 1999, Sato-Okoshiet al.
2008), were identified as important pests in 5off-shore systems. In
at least 3 of these instances thehosts did not develop from natural
spatfall and hadbeen transported from nursery systems (Lleonart
etal. 2003, Simon 2015). It is therefore possible thatthe worms had
reached the culture systems artifi-cially, and, once established, a
large local popula-tion could develop in the same way as proposed
foron-shore culture systems. It is, however, still possi-ble that
the hosts had been infected by free-swim-ming larvae (Williams
2015). The absence of pestswith adelphophagic or lecithotrophic
larvae in thenear-shore and intertidal is unexpected; if thesource
population is inter- or subtidal, the relativeproximity to the
cultured subtidal molluscs shouldenable infestations by such
larvae.
Planktotrophy
Planktotrophic larvae are particularly well suitedto infest
molluscs in the off-shore for 3 reasons.Firstly, they are produced
by the thousands perbrood and should therefore be common
componentsof the plankton. For example, Abe et al. (2014) re
-corded up to 5000 larvae m3 of P. onagawaensis atup to 5 m depth
in Onagawa Bay. Secondly, these lar-vae usual ly spend 3 to 4 wk in
the water column (e.g.Blake & Arnofsky 1999, David & Simon
2014, Davidet al. 2014) which would increase their opportunitiesfor
reaching off-shore systems. Finally, plankto -trophic larvae are
usually active swimmers until theybecome too heavy and are ready to
settle (Hansen etal. 2010). Together with movement by water
cur-rents, these characteristics should enable plankto -trophic
larvae to reach molluscs in off-shore culturein high enough numbers
to become problematic eventhough larval mortality may be high.
Intensive cul-ture in near-shore and off-shore systems may
further
enhance the successful recruitment of planktotrophiclarvae by
providing substrates which would other-wise not be available in the
area.
Buck et al. (2005) and Brenner et al. (2009) con-cluded that the
dilution of polydorid larvae due todistance from near-shore source
populations signifi-cantly reduced the susceptibility of mussels,
Mytilusedulis, in off-shore suspended culture to infestation.These
distances (11 to 27 km) were, however, con-siderably greater than,
for example, in South Africaand Japan (1 km, Williams 2015; W.
Sato-Okoshipers. obs.), and probably other countries too, andcould
ac count for the different findings. Buck et al.(2005) also
suggested that the short planktonicphase of the polydorid, which
they identified as P.ciliata (2 wk planktonic phase, as described
by Daro& Polk 1973; but see also Problems with taxonomybelow),
also played a role. Undoubtedly, here theeffects of a short
planktonic phase and the greatdistance off-shore were further
exacerbated by asmall source population where only 1.7 to 2.7%
ofthe samples were infested by a mean of up to 6worms per infested
shell (Buck et al. 2005, Brenneret al. 2009). Larger source
populations that arecloser to the culture systems and composed of
spe-cies with longer planktonic phases would pose agreater risk
(e.g. P. brevipalpa infesting wild andcultured Patinopecten
yessoensis in Abashiri Bay[Sato-Okoshi & Abe 2012], and P.
onagawaensisfound on farmed scallop and wild abalone in thesame
localities [Sato-Okoshi & Abe 2013]).
Poecilogony
Poecilogony is a rare reproductive dimorphism(Chia et al. 1996,
David et al. 2014). A perceivedadvantage to poecilogony for pest
polydorids is thatthey may benefit from dispersal by the plankto
-trophic larvae to the off-shore systems, and the laterdevelopment
and maintenance of local populationsby the adelphophagic larvae
(Chia et al. 1996, David& Simon 2014, David et al. 2014).
However, the typeof poecilogony could affect the ability of a
species tobecome established in off-shore systems as a con
-sequence of the final number of larvae that meta -morphose.
Poecilogony was recently described forP. hop lura from South
Africa, with females producingeither planktotrophic or
adelphophagic larvae(David et al. 2014). Purely planktotrophic
broods ofP. hoplura contain more than a thousand larvae whilepurely
adelphophagic broods contain a mean of 20(David et al. 2014). In
Simon (2015), all the develop-
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Aquacult Environ Interact 7: 147166, 2015158
ing broods observed in the off-shore containedplanktotrophic
larvae, while all those from the on-shore populations contained
adelphophagic larvae.The larval type of females not brooding at the
time ofsampling was not determined, so it is possible thatthey
produced different types of larvae, since mixedpopulations have
been found (David 2015). This sug-gests that in South Africa at
least, off-shore popula-tions may have been established by
planktotrophiclarvae and then maintained by later generations
offemales producing adelphophagic larvae. By con-trast,
poecilogonous species producing both larvaltypes simultaneously
appear not to capitalise on thedual advantages of different larval
types, as evi-denced by the low number of records of poecilo
-gonous pests in off-shore culture systems. This mightbe a
consequence of inter-sibling competition. Inmixed broods of
Boccardia proboscidea, plankto -trophic larvae are often
cannibalised by theiradelpho phagic siblings, reducing the number
of dis-persive larvae entering the water column (David &Simon
2014). Furthermore, planktotrophic larvae inmixed broods lack
swimming chaetae which mayinhibit their swimming abilities compared
to that oflarvae from pure broods (Gibson 1997). This mightalso
apply to other species which produce mixedbroods.
The high incidence of pests with planktotrophiclarvae may be
because the larvae are produced insuch high numbers that they
out-compete specieswith adelphophagic larvae. Alternatively, or
addi-tionally, it may reflect the fact that many polydoridspecies
produce planktotrophic larvae. Of the spe-cies included in this
review for which the larvaldevelopmental modes are known, 62.5%
produceplanktotrophic larvae, 8.3% each produce adelpho -phagic or
lecithotrophic larvae or are poecilogo-nous, with a further 12.5%
having different modesin different records (Table 1). These
proportionsare very similar to those found among the Boccar-dia,
Boccar di ella, Dipolydora and Polydo ra species;59, 21 and 3%
produced plankto trophic,adelphophagic and lecithotrophic larvae,
respec-tively, while 16% were poecilogonous (Blake &Arnofsky
1999). These proportions are also similarto that of individual
records of polydorids in differ-ent culture systems (Table 2):
planktotrophy (68%),adelphophagy (16%), lecitho trophy (2%) and
poe-cilogony (14%). Thus the high incidence of pestspecies
producing planktotrophic larvae in theintertidal, near-shore and
off-shore may be a pro-portionate representation of species with
plank-totrophic larvae among the polydorids. However,
the disproportionately high number of records foradelphophagic
and poecilogonous developmentamong species recorded as pests in
on-shore facili-ties supports the hypothesis that some se
lectiondoes occur there (e.g. P. hoplura, B. pro bos cideaand
Boccardia pseudonatrix in South Afri ca [Simon2015], P. uncinata
and B. pseu do natrix [as B. knoxi,Sato-Okoshi et al. 2008] in
Australia and P. uncinatain Japan [Sato-Okoshi et al. 2015]).
Host and culture system
The link between larval development and peststatus of worms in
different culture systems may befurther enhanced by the culture
period of the hostsin the different systems. Thus the dominance of
spe-cies with larvae that emerge at a late stage of devel-opment in
on-shore culture systems may also berelated to the fact that 16 of
the 22 records in on-shore facilities included in this study were
of slow-growing aba lone which remain in culture for >4
yr(Castell 2012). This would facilitate the accumula-tion of many
polydorids (Pregenzer 1983) and overmany generations; e.g. B.
proboscidea start repro-ducing within about 1 mo of settling and
live forapprox. 1 yr, during which time they produce manysuccessive
broods, leading to almost constantrecruitment on farmed abalone
(Simon & Booth2007; see also Sato-Okoshi et al. 2015, for
moreexamples). Thus, when hosts remain in culture forseveral years,
exponential growth of the worm pop-ulation can be expected if
conditions re main thesame or effective remedial measures are not
taken.Conversely, 18 of the 39 records of off-shorecultures were of
oysters and mussels that re main inculture for
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Simon & Sato-Okoshi: Polydorid polychaete pests on cultured
molluscs
GLOBAL SPECIES DIVERSITY, DISTRIBUTION,HOST SPECIFICITY AND
TAXONOMY
Movement of pests with molluscs in aquaculture
Reviews that consider polydorids in general, andshell-infestors
associated with cultured molluscs inparticular, usually have a
regional focus: Chile (Sato-Okoshi & Takatsuka 2001, Moreno et
al. 2006), SouthAfrica (Simon et al. 2006, Boonzaaier et al.
2014,Simon 2015), Japan (Sato-Okoshi 1999, Sato-Okoshi& Abe
2013), Korea (Sato-Okoshi et al. 2012), China(Zhou et al. 2010,
Sato-Okoshi et al. 2013), Australia(Blake & Kudenov 1978,
Sato-Okoshi et al. 2008,Walker 2011, Walker 2014), New Zealand
(Read2004) and the United States of America (e.g. Blake1969b).
These often indicate the presence of speciesthat are outside of
their natural distribution ranges,but there is no comprehensive
global review of theshell-boring polydorid pests of cultured
molluscs.
The movement of molluscs for aquaculture hasbeen implicated in
the inadvertent spread of manyalien species, including polychaetes
(e.g. Wolff &Reise 2002, McKindsey et al. 2007, Ruesink et
al.2005, Haupt et al. 2012, inar 2013). In particular,Haupt et al.
(2012) demonstrated that even aftercleaning, oysters still
harboured polydorid shell-borers after translocation. Yet the
records which con-firm oysters and abalone as the vectors of
transporta-tion are limited; Polydora websteri and
Boccardiaproboscidea were transported from mainland USA toHawaii
(Bailey-Brock & Ringwood 1982, Bailey-Brock 2000), P. uncinata
from Japan to Chile (Rada-shevsky & Olivares 2005), and
probably P. websterifrom Namibia to South Africa (Simon 2015,
Williams2015), while the sabellid Terebrasabella heterounci-nata
was transported from South Africa to Californiaand further (Culver
et al. 1997, Moreno et al. 2006).In some instances aquaculture may
not have beenthe vector of introduction of a pest to a new
region,but is responsible for its spread within its introducedrange
(e.g. Simon et al. 2009, Haupt et al. 2012,Williams 2015). Despite
this close association be -tween polydorid polychaetes and cultured
molluscs,reviews of the contribution which aquaculture makesto the
movement of aliens pay little or no attention topolydorids (e.g.
Wolff & Reise 2002, Ruesink et al.2005, McKindsey et al.
2007).
This neglect might be because molluscs would betreated against
polydorids in general rather than anyspecific species (Royer et al.
2006), rendering theidentification of individual pest species
meaninglessto many farmers. The neglect would be further exac-
erbated by the many taxonomic problems associatedwith polydorids
(Sato-Okoshi et al. 2015). However,the failure to identify species
means that their spreadbeyond their natural distribution ranges is
often onlynoticed after they have become established and arethen
almost impossible to eradicate (Bailey-Brock1990).
Results and discussion
A total of 178 records from the literature andauthors un
published data identified 38 polydoridspecies (8 Boccardia spp., 1
Boccardiella sp., 11 Di -poly dora spp., 17 Polydora spp., 1 Pseudo
polydorasp., excluding those that had only been identified togenus
level), infesting 36 cultivated or commerciallyharvested mollusc
species in 25 countries on all con-tinents except Antarctica (Table
1). Half the speciesconsidered in this review are, or have the
potential tobe, problematic alien species. The most virulent
ofthese are undoubtedly P. websteri, P. uncinata, P.haswelli and P.
hoplu ra, which collectively infest 21hosts in 17 countries. Among
these species, P. unci-nata was always considered a pest (in 15
records)while P. hoplura, P. websteri and P. has welli
wereconsidered pests in approximately half of theinstances where
they were reported with culturedmolluscs (Table 1). Twelve species
were re corded in2 countries and 21 in only one. Eighteen species
wereassociated with commercially important molluscsonly within the
native range of the polychaete, 8were recorded within and outside
of their nativeranges, and 9 were recorded only outside of
theirnative ranges. From among these species, where theproportion
of records as pests exceeded 50%, themaximum total number of
records was 8. Thirteenspecies were never recorded as pests (Table
1).Among the species infesting only 1 host, only Boccar-dia
semibranchiata, infesting Crassostrea gigas, wasrecorded in more
than one country (France andSpain). Of the species that infested
more than 2 hosts,11 were restricted to either one country, or
oneregion (e.g. P. onagawaensis has only been found inChina and
Japan, and P. aura has only been found inJapan and Korea, while P.
rickettsi which, althoughrestricted to South America, was recorded
in Chile,Argentina and Brazil).
inar (2013) suggested that 36 of the 292 alienpolychaete species
that he reviewed were probablymoved by aquaculture, including 1
sabellid and 15polydorid shell-borers. However, he
undoubtedlyunderestimated the full extent of the distribution
of
159
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Aquacult Environ Interact 7: 147166, 2015160
these pests as he only considered records whereworms were
specifically identified as alien; for exam-ple, he did not list P.
hoplura as an alien in Australia,although it had already been
recorded there severaltimes (Blake & Kudenov 1978, Hutchings
& Turvey1984, Lleonart et al. 2003). Our tally has increasedthe
number of known alien shell-infesting polydoridsto 17, with the
addition of Boccardia chilensis and Di -po ly dora concharum.
Furthermore, the alien rangesof 9 species have been extended
(Boccardiella ha ma -ta, Boc car dia polybranchia, Boccardia
pseudonatrix,D. armata, D. concharum, P. ciliata, P. haswelli,
P.hoplura, P. rickettsi and P. websteri) while
Boccardiasemibranchiata and P. hoplura should be
consideredcryptogenic, rather than alien, on the Atlantic coastof
Europe (cf. inar 2013 and Haydar & Wolff 2011).
Relationship between aquaculture and the spread ofalien
species
Although there are few instances where the move-ment of molluscs
for aquaculture was the confirmedvector for the transport of
polydorids, this reviewconfirms the conclusions of previous authors
thataquaculture is an important vector and reservoir ofexotic
species, including polychaetes (e.g. Wolff &Reise 2002, inar
2013). Linear regressions showedsignificant positive relationships
between the num-ber of hosts cultured in a country and the number
of(1) shell-infesting, (2) non-indigenous polydo rids and(3)
non-indigenous pest polydorids recorded percountry (Table 3).
Furthermore, a positive significantrelationship was found between
the number of non-indigenous shell-boring polydorid species and
thenumber of shell-boring non-indigenous pests re -corded on
commercially reared hosts, per country(Table 3). For the latter
analysis, cryptogenic species(such as P. hoplura in France and
Belgium) wereomitted, as were species identified only to genuslevel
and references to P. ciliata because their alienstatus could not be
confirmed. In spite of a small sam-
ple size, these analyses provide a telling indictmenton the role
which aquaculture plays in the spreadand flourishing of alien pest
polydorid species. Thisconclusion is further reinforced by the fact
that themost non-indigenous pests were recorded in Japan,which also
cultivated the most hosts (e.g. Sato-Okoshi & Nomura 1990,
Sato-Okoshi 1999, Sato-Okoshi & Abe 2012, 2013). Additionally,
all of thepest polydorids associated with cultured oysters
inAustralia (Walker 2014), 5 of the 6 species in Chile(Moreno et
al. 2006) and 3 of the most importantpests in South Africa
(Boonzaaier et al. 2014, Simon2015, Williams 2015) are alien.
Host specificity
Although host species was identified as a factor indetermining
pest species, shell-infesting polydoridsare usually not
host-specific (Moreno et al. 2006, Sato-Okoshi et al. 2008, Simon
2011, 2015). This is sup-ported by this review. Eight of the 37
species infestedmore than 4 hosts, with P. websteri, P. haswelli,
P. un-cinata and P. hoplura recorded on 6 or more hosts(Table 1).
Eleven and 13 species were re corded on 2hosts or one host, re
spectively, when unidentified spe-cies are ex cluded. The species
which were recordedon only one host may in fact represent a
restricted dis-tribution range of the worm since some of these
spe-cies were recorded only in one country or region each(e.g. B.
semibranchiata, D. albo rec talis), while othershave been recorded
on other hosts which are not com-mercially important (e.g. D.
socialis, D. concharum,Blake 1971). Similarly, 10 species infested
only bi-valves but this might reflect the situation on farmsrather
than host specificity (Table 1); for example, P.websteri has only
been recorded on bivalves in cul-ture, but also on gastropods in
the wild (Blake 1971)while, D. armata has only been found on
farmedabalone, but is not restricted to gastropods in the wild(e.g.
Sato-Okoshi 1999). One exception is D. capensis,which has been
recorded widely on wild and farmed
gastro pods in South Africa butnever on oysters, even
whenpresent on aba lone close by (Si-mon 2011, 2015). The
physicalstructure of the host may, how-ever, affect its
susceptibility toinfestation. For example, the ru-gose nature of
the shell of C. gi-gas is believed to contribute to
itseffectiveness at creating habitatsfor other organisms (Haydar
&
Equation (n) R2 p
Polydorids vs. hosts y = 0.24 + 1.24x (25) 0.651
-
Simon & Sato-Okoshi: Polydorid polychaete pests on cultured
molluscs 161
Wolff 2011). Similarly Haliotis midae is infested bymore species
(Boonzaaier et al. 2014) than any otherhaliotid included in the
present study and this may bea consequence of the rugose nature of
its shell com-pared to that of other haliotids (Fig. 2).
Problems with taxonomy
An important outcome of this review is that it hashighlighted
the species for which identifications are(probably) problematic.
Since its initial identificationas a pest of oysters by Haswell
(1885), B. poly-branchia has been recorded as a pest of C. gigas
inFrance (Ruellet 2004, Royer et al. 2006) and My ti lusedulis in
Australia (Pregenzer 1983). There is, how-ever, much confusion in
the literature around thisspecies (Blake & Kudenov 1978, Simon
et al. 2010)and it probably includes several morphologicallysimilar
species. Additionally, it has not beenrecorded with oysters in
Australia since 1983 (Pre-genzer 1983, Walker 2014), while the
photographprovided in Ruellet (2004, their Fig. 50), though notvery
clear, more closely resembles B. proboscidea,which has also been
recorded on the Atlantic coastof Spain (Martinez et al. 2006), in
Roscoff, France (T.Struck & C. A. Simon unpubl. data) and
Belgium(Kerckhof & Faasse 2014). It is therefore possible
thatthe identifications of this species as a pest are incor-rect.
Similarly, P. ciliata was originally described insediment (Johnston
1838) and its identification as ashell-borer is therefore very
controversial. Blake(1971) and Blake & Kudenov (1978) suggested
that P.ciliata infesting cultured molluscs on the east coast
ofNorth America and in Australia were probably P.websteri. Later,
Mustaquim (1988) demonstrated thatshell-boring P. ciliata in Europe
were molecularlydistinct from non-boring forms; yet P. ciliata has
beenidentified as a shell-borer several times since 1988, in
Europe, India and China (our Table 1, Gao et al.2014), thus
perpetuating earlier errors.
Recent morphological and molecular analyses sug-gest that
extensive revision to 3 important pest spe-cies is necessary. Here
we identified P. websteri asthe most wide-spread shell-boring
polydorid. How-ever, recent molecular analysis suggested that
P.websteri from near the type locality is molecularlydistinct from
conspecifics in southern Africa, Japanand Australia, suggesting
that at least these latterrecords represent a different species
which Williams(2015) referred to P. cf. websteri. Additionally, it
isun certain whether P. websteri in Brazil (Sabry &Magalhes
2005) should be referred to P. haswelli(see Rada shevsky et al.
2006). Thus the records con-sidered here of P. websteri may
actually representseveral species. To further complicate matters,
pre-liminary molecular investigations also suggest that P.ona ga wa
ensis may be synonymous with P. websteri(Williams 2015).
Additionally, studies by Read (2010),Walker (2014) and Williams
(2015) provide compell -ing arguments for synonymising shell-boring
P. has -welli with P. neocaeca and P. uncinata with P. hop lu -ra.
If they are right, the known distribution of thesespecies will
change considerably, and P. hoplura willbe the most widespread pest
in the world.
The literature reviewed here also included 7 Poly-dora, 2
Boccardia and 3 Dipolydora species identifiedonly to genus level.
Given the frequency with whichpolydorids may be moved with
aquaculture and ship-ping (inar 2013), it is imperative that pest
polydoridworms be identified properly. This will increase
ourunderstanding of the actual movement and distribu-tion of
shell-infesting polydorids and help identifynew alien species in
time to enable eradicationbefore the worms become established. It
is clear thatpolydorids can be difficult to identify, especially
formany aquaculturists who lack taxonomic trainingand access to the
literature. For example, South Afri -
Fig. 2. (A) Haliotis midae, (B) H. gigantea and (C) H. discus
hannai showing the difference in the rugosity of the abalone shells
(scale bars = 2 cm), which can influence the species susceptibility
to infestation by polydorid species
-
Aquacult Environ Interact 7: 147166, 2015162
can farmers initially assumed that locally culturedabalone were
infested by a Polydora species, whenthey were, in fact, infested by
P. hop lu ra, B. probos -cidea and D. capensis (Simon et al. 2006,
Simon et al.2010). It is therefore imperative that an
alternativemeans to identify worms is developed, and that
amolecular database of polydorids, using commonDNA markers such as
18S rRNA, 28S rRNA and COI,be generated. Such a database will
facilitate therapid identification of pests, even when regional
tax-onomic expertise is lacking.
CONCLUSIONS
Observations of the larval developmental modes ofpolydorid pests
of cultured molluscs in South Africa(Simon 2015) suggested that
molluscs grown in on-shore culture systems are more likely to be
infested byspecies producing larvae which leave the maternalburrow
at a late stage of development while those inoff-shore culture
systems would be infested byspecies producing larvae with a longer
planktonicphase. Our review of the literature reporting the
peststatuses and larval developmental modes of poly-dorids
infesting cultured (or commercially harvested,wild) molluscs
suggest that these observations arevalid on a more global scale.
However, a more com-plete analysis is hampered by several
confoundingfactors. (1) Polydorids are usually investigated
onlywhen they become problematic, and many countriesare therefore
presumably not experiencing problemswith infestations. For example,
Crassostrea gigas iscultured in more than 50 countries (Ruesink et
al.2005, Castell 2012), but we found records of infestationfor just
a third of that. This does not necessarily meanthat oysters in the
remaining countries are free ofpolydorids, just that they have not
been investigated.Thus the rare and common polydorid species
wouldprobably have been under-represented in the analy-sis. (2)
Polydorids are sometimes investigated duringtargeted research by
taxonomists, but the pest statusof the worms may not always be
indicated (e.g. Blake1971, Walker 2014). Furthermore, the positive
rela-tionship between the numbers of shell-boring poly-dorid
species and cultured hosts examined percountry may be influenced by
the level and number oftaxonomic studies conducted in different
countries.For example, since the 1990s, one of the authors
(W.Sato-Okoshi) has re corded 15 polydorid species asso-ciated with
9 cultured mollusc species in Japan (e.g.Sato-Okoshi & Nomura
1990, Sato-Okoshi 1999, Sato-Okoshi & Abe 2012, 2013).
Similarly, many polydorid
species (in cluding non-indigenous and pest species)have been
recorded in South Africa (14; e.g. Boonza-aier et al. 2014,
Williams 2015), Australia (9; Blake &Kudenov 1978, Skeel 1979,
Sato-Okoshi et al. 2008,Walker 2014), New Zealand (7; Handley &
Bergquist1997, Read & Handley 2004, Read 2010), Chile
(6;Sato-Okoshi & Takatsuka 2001, Moreno et al. 2006)and Brazil
(5; Radashevsky et al. 2006). In contrast,only 4 polydorid species
have been re corded in China,on 5 hosts (Zhou et al. 2010,
Sato-Okoshi et al. 2013).Since China is the leading producer of
molluscs glob-ally, culturing at least 11 species (Castell 2012,
Lucas2012), this is undoubtedly an underestimate of theshell-boring
polydorids in that country. (3) Certain cul-ture methods have been
used more frequently thanothers. Among the re cords considered
here, off-shoresuspended culture was the most frequently used (for
14species in 24 countries), followed by near-shore culture(13
species in 13 countries), on-shore (11 species in 13countries) and
intertidal culture (5 species in 12 coun-tries). The apparent
preference for off-shore sus-pended culture may have biased the
analyses.
To fully understand regional polydorid species di -ver sity and
the risk of species becoming pests orbeing moved along with their
hosts, polydorid infes-tations must be surveyed under cultured and
naturalconditions. Species which are benign in their nativeranges
may become pests when translocated to a newregion or exposed to
novel hosts, as did B. pro-boscidea in South Africa. While we
provide strong ev-idence suggesting that larval developmental
modedetermines which species will become pests (particu-larly in
on-shore systems), other life history character-istics may also
play a role, such as the life span andthe timing and duration of
the reproductive and set-tlement periods (i.e. the longer the more
severe theinfestation). Such information will enable
aquacultur-ists to predict which species could become problem-atic
while knowl edge of the timing of the settlementof juveniles will
allow the timeous implementation ofcontrol measures.
Acknowledgements. The authors thank Natasha Mothapofor her
advice and help with the statistical analyses andAndrew David and
Matt Bentley for their valuable com-ments on the manuscript.
C.A.S.s visit to Japan was fundedby the HB & MJ Thom and
Oppenheimer Memorial Trusttravel grants and research funds were
provided by theNational Research Foundation (Thuthuka Programme).
Thefunding bodies made no contribution to the development ofthe
study, the interpretation of the data or the preparationand
submission of the manuscript. C.A.S. also thanks thestaff and
students of the Laboratory of Biological Oceanog-raphy, Tohoku
University, Sendai, for their hospitality dur-ing her stay.
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Simon & Sato-Okoshi: Polydorid polychaete pests on cultured
molluscs
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