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AQUACULTURE ENVIRONMENT INTERACTIONS
Aquacult Environ Interact
Vol. 11: 291–304, 2019
https://doi.org/10.3354/aei00314 Published June 27
1. INTRODUCTION
Aquaculture is a rapidly growing industry world-
wide, with production expected to surpass the wild
fishery catch by 2025 (FAO 2015). As aquaculture has
intensified, diversified and expanded into new geo-
graphic areas, diseases have become an increasingly
important constraint on production. Transboundary
and emerging diseases are considered to be major
limiting factors for continued expansion of global
aquaculture production and trade (Hedrick 1996,
Subasinghe 2005, Whittington & Chong 2007, Oidt-
mann et al. 2011). Losses due to disease have been es-
timated to be greater than US$3 billion per annum in
Asia alone (Vallat 2017). In marine shellfish (mollus-
can) aquaculture, pathogens and parasites can result
in serious financial, social and environmental impacts,
whose nature and magnitude vary widely between lo-
cations and species. For example, an Ostreid her-
pesvirus type 1 (OsHV-1) microvar caused mass mor-
talities of spat and adult Pacific oysters Crassostrea
gigas in both hemispheres (Renault et al. 2000,
Segarra et al. 2010, Peeler et al. 2012, Bingham et al.
2013, Paul-Pont et al. 2013). The parasite Marteilia re-
fringens (sensu lato, infecting oysters and mussels) is
known to cause serious mortality outbreaks in cul-
© The authors 2019. Open Access under Creative Commons by
Attribution Licence. Use, distribution and reproduction are un -
restricted. Authors and original publication must be credited.
Publisher: Inter-Research · www.int-res.com
*Corresponding author: steve.webb@cawthron.org.nz
ABSTRACT: The endemic green-lipped mussel (GLM) Perna canaliculus is a key cultural and
economic species for New Zealand. Unlike other cultured shellfish species, GLMs have experi-
enced relatively few disease issues. The apparent absence of diseases in both wild and farmed
GLM populations does not preclude risks from environmental changes or from the introduction of
overseas mussel pathogens and parasites. Potential for disease exchange between the GLM and
other mytilid species present in New Zealand has yet to be elucidated. After reviewing and dis-
cussing relevant scientific literature, we present an initial assessment of GLM vulnerability to dis-
ease threats and the potential risk pathways for mussel pathogens and parasites into New Zealand
and highlight a number of challenges. These include knowledge gaps relevant to GLM suscepti-
bility to exotic pathogens and parasites, risk pathways into New Zealand and biosecurity risk
associated with domestic pathways. Considerations and findings could potentially apply to other
farmed aquatic species with limited distribution range and/or low disease exposure.
KEY WORDS: Mussel · Disease · Shellfish · Risk pathways · Risk management · Biofouling
O
PEN
PEN
A
CCESS
CCESS
REVIEW
Disease threats to farmed green-lipped mussels
Perna canaliculus in New Zealand: review of
challenges in risk assessment and pathway analysis
A. Castinel1,4, S. C. Webb1,*, J. B. Jones2, E. J. Peeler3, B. M. Forrest1
1Cawthron Institute, Nelson 7010, New Zealand
2Murdoch University, Murdoch, Western Australia 6150, Australia
3Centre for Aquaculture Fisheries and the Environment, Weymouth DT4 8UB, UK
4Present address: PO Box 5142, Nelson 7010, New Zealand
Aquacult Environ Interact 11: 291– 304, 2019
tured European flat oysters Ostrea edulis, but its im-
pact in farmed mussels Mytilus galloprovincialis is re-
portedly limited to condition loss and moderate mor-
tality (Villalba et al. 1993, Pérez Camacho et al. 1997).
The noticeable increase in the occurrence of aqua -
tic diseases in recent years highlights the need to
better understand the health of both aquaculture and
wild populations of marine shellfish as well as the
contributing factors (Harvell et al. 1999, Murray &
Peeler 2005, Peeler et al. 2011). Opportunistic patho-
gens, such as Vibrio spp., have been implicated in
mussel mortality events, often taking advantage of
variations in water temperature or salinity weaken-
ing the hosts (Romero et al. 2014). Direct impacts of
diseases, such as mortality, can be monitored and
quantified, whereas indirect effects can be of equal
or greater importance but are more difficult to meas-
ure. Effects include decreased availability of wild
spat, lower end-product value, difficulties accessing
markets, costs of disease control to both government
(e.g. eradication and laboratory testing for surveil-
lance) and industry (e.g. restriction on movements of
live shellfish) and indirect impacts on the community
and local economy (Israngkura & Sae-Hae 2002,
Evans 2006).
In contrast with other cultured shellfish around the
world, New Zealand’s endemic green-lipped mussels
(GLMs) Perna canaliculus (farmed under the trade-
mark GreenshellTM mussels) have experienced rela-
tively few disease issues. GLMs are, economically, the
most important aquaculture species in New Zealand,
where production is around 94 000 t annually (which
represents ca. NZ$300 million of annual sales), and
several thousand hectares of water space across 6
temperate coastal or offshore growing regions are oc-
cupied (Fig. 1). Beyond its marketable value, the
green-lipped mussel, or ku¯ tai, is an iconic species pro-
tected by New Zealand’s indigenous Ma¯ori through
their kaitiakitanga, or guardianship of the natural en-
vironment. Various endemic pathogens and parasites
have been reported for this species, but with the ex-
ception of the condition described as digestive epithe-
lial virosis (DEV; Jones et al. 1996), there is no evi-
dence of any major impact on cultured or wild mussel
populations in New Zealand (Webb 2013).
The reason for the absence of significant health
issues in the GLM is unclear. The disease vulnerabil-
ity of Perna species is poorly understood compared to
other mytilid species. Perna as a genus is confined to
the South Atlantic and Indo-Pacific regions and has
not been farmed outside of its natural geographic
range. As such, opportunities for intensive aquacul-
ture, exposure to new disease agents and subsequent
clinical expression have been relatively limited. The
apparent healthy status of the GLM population could
reflect some inherent resilience of the species or a
lack of exposure to exotic pathogens due to New
Zealand’s geographic isolation. However, this appar-
ent absence of diseases in GLMs needs to be placed
within context: first, there is currently no legal re -
quirement for on-farm surveillance, and second,
there are no industry-wide standards on acceptable
levels of mortality that trigger official reporting and
subsequent animal health investigation.
Assessment of potential disease threats to the
GLM, and associated uncertainties, is a first step to -
wards identifying the need for, and scope of, appro-
priate management interventions. As such, this
paper re views the vulnerability of the GLM to dis-
ease threats and provides an overview of potential
risk pathways for mussel pathogens and parasites
into New Zealand. The approach follows guidelines
for risk analysis set out by the World Organisation for
Animal Health (OIE 2017). Hazard identification
takes into account existing records of disease agents
and pathological conditions in New Zealand as well
as potential exotic agents. Pathways for the introduc-
292
Fig. 1. Main locations of green-lipped mussel aquaculture
areas in New Zealand, illustrating their proximity to interna-
tional shipping ports (circles)
Castinel et al.: Disease threats to green-lipped mussels
tion of pathogens and parasites from outside New
Zealand (release assessment) and their spread within
the country (part of the consequence assessment) are
considered separately. Risk mitigation is discussed in
relation to present and potential border controls and
domestic risk pathway management. We also iden-
tify some of the broader challenges for risk assess-
ment and management, which may apply to the
aquaculture of other species with limited global dis-
tribution and/or currently limited disease exposure.
2. ACTUAL OR POTENTIAL DISEASE THREATS
FOR GREEN-LIPPED MUSSELS
2.1. Existing records of pathogens, parasites and
pathological conditions
The known pathogens, parasites and pathological
conditions of GLM and other cultured or wild shell-
fish species in New Zealand have been reviewed
(Webb 2013, Georgiades et al. 2016). Findings are
largely based on sporadic screening of commercial or
wild stocks (e.g. in response to unexplained mort -
ality) and local ad hoc surveillance. As there has
been no systematic or comprehensive national sur-
veillance programme of shellfish diseases to date,
existing knowledge is unlikely to provide a complete
picture (Castinel et al. 2014). Webb et al. (2019) re -
cently published a consolidation of histological
findings from more than 3200 mussel specimens
gathered from key production areas around New
Zealand between 2007 and 2016. The authors turned
the opportunistically collected data into valuable
baseline information on pathogens, parasites and
conditions of the GLM and Mytilus galloprovincialis
(Table 1a,b). The latter mussel species is not commer-
cially farmed in New Zealand, but it is a significant
component of the biofouling assemblage on GLM
farms (Forrest & Atalah 2017) and has the potential to
play a role in the exchange of pathogens and para-
sites with GLMs.
GLMs harbour a range of enzootic disease agents
as well as parasites such as rickettsiae and apicom-
plexan parasite X (Hine 2002, Webb 2013). With the
exception of DEV being associated with significant
spat mortality in the early 1990s (Jones et al. 1996),
none of these organisms or conditions are known to
have a significant impact on the health of farmed
GLMs, wild conspecifics or other shellfish in New
Zealand (Castinel et al. 2014). Even for DEV, the
actual impact on mussels and other bivalve species,
its prevalence in farmed GLMs and potential costs to
the aquaculture industry have not been comprehen-
sively evaluated. Further, in spite of histopathologic,
transmission electron microscopy and molecular evi-
dence suggesting a viral infection (Jones et al. 1996,
Webb 2013), the aetiology of DEV remains obscure.
2.2. Challenges for hazard identification of
potential threats
Determining, in a systematic way, the future dis-
ease threats to GLM aquaculture is a significant chal-
lenge. As the GLM is the only Perna species in New
Zealand and occurs nowhere else in the world, its
susceptibility to new pathogens and parasites is
unknown. Furthermore, only 2 other species in the
Perna genus are known to exist globally: P. viri dis in
the Indo-Pacific region (FAO 2017) and P. perna in
the tropics, subtropics and, recently, Gulf of Mexico
(GISD 2019). Although these are cultivated or har-
vested in many countries, knowledge of disease
occurrence and susceptibility is sparse (Vakily 1989,
Lasiak 1993, Kaehler & McQuaid 1999, da Silva et al.
2002, Galvao et al. 2015, FAO 2017).
In the absence of data, a precautionary approach
assumes that pathogens of closely related cultured or
wild bivalves are also potential hazards to the GLM.
Pathogen exchange between the GLM and M. gallo -
provincialis (or closely related shellfish) is therefore
plausible, given that, of the 17 main agents recorded
in GLMs, 15 also occur in M. galloprovincialis, 9 in
Crassostrea gigas and 10 in Ostrea chilensis in New
Zealand (Table 1a). Host shifting by pathogens could
be enabled by a number of drivers, including host
relatedness, geographic overlap, changes in host−
environment interactions and disease ecology, and
anthropogenic factors (Peeler & Feist 2011, Engering
et al. 2013).
It is of particular interest whether the GLM might be
susceptible to organisms that are not found in New
Zealand but which cause mortalities in wild or cul-
tured M. edulis species complex overseas, including
in the Mediterranean mussel M. galloprovincialis
(Vill alba et al. 1993, Pérez Camacho et al. 1997, Krish-
nakumar et al. 1999, Ray yan et al. 2006, Romero et al.
2014). Of at least 6 significant disease agents that have
been described for Mytilus spp. internationally, none
has yet been recorded in New Zealand (Table 1b).
However,evidence ofongoing human- mediated trans-
port of Mytilus spp. into New Zealand from the North-
ern Hemisphere (Gardner et al. 2016) raises the possi-
bility of new arrivals introducing exotic pathogens to
which the GLM is susceptible (Ray yan et al. 2006).
293
Aquacult Environ Interact 11: 291– 304, 2019
294
(a) Pathogens recorded in NZ mussels Perna canaliculus and Mytilus galloprovincialis and other NZ shellfish hosts and their associated impact
Main group Name Occurrence in Occurrence in other NZ hosts Impact in NZ shellfish
P. canaliculus and/or
M. galloprovincialis
Virus, clone Disseminated hemic M. galloprovincialis Flat oyster Ostrea chilensis No clinical impact observed
or mutagen tagen neoplasia only
Virus (putative Digestive epithelial virosis Both species Scallop Pecten novaezelandiae, Ubiquitous with high intensity in scallops;
aetiology) rock oyster Saccostrea glomerata high mortality reported in P. canaliculus
in early 1990s
Bacteria Rickettsia and Chlamydia Both species Numerous shellfish species Common; potential threat in high-density
culture
Bacteria Vibrio spp. Both species Numerous shellfish species Opportunistic pathogenic role for Vibrio
splendidus
Fungus Microsporidium rapuae Both species Flat oyster O. chilensis No clinical impact observed
Protozoa Apicomplexan parasite X Both species Pacific oyster Crassostrea gigas, No clinical impact observed in mussels,
flat oyster O. chilensis but predisposition for bonamiasis in flat oysters
Protozoa Other apicomplexans, Both species Pacific oyster C. gigas, flat oyster No clinical impact observed
e.g. Nematopsis sp. O. chilensis
Protozoa Invasive ciliates Both species Pacific oyster C. gigas, flat oyster No clinical impact observed
O. chilensis
Protozoa Ciliates (other) Both species Pacific oyster C. gigas, flat oyster No clinical impact observed
O. chilensis
Protozoa Perkinsus olseni P. canaliculus only Abalone Haliotis iris and other Possible clinical impact obscured by copepod
shellfish species infection in digestive gland
Platyhelminthes Paravortex sp. Both species Scallop P. novaezelandiae Ubiquitous; no clinical impact observed
(Turbellaria) and other shellfish species
Platyhelminthes Other flatworms Both species Numerous shellfish species Opportunistic pathogen, only significant with
(Turbellaria) (Enterogonia orbicularis, heavy infestation
and putative planocerid)
Platyhelminthes Bucephalus sp. P. canaliculus only Flat oyster O. chilensis Impact unclear
(Digenea)
Table 1. Main pathogens and parasites recorded (a) in New Zealand (NZ) and (b) overseas in mussel species and other susceptible shellfish hosts. See Webb et al.
(2019) for details of prevalence and impacts in NZ hosts. This does not include pathogens that can be vectored by mussels
Castinel et al.: Disease threats to green-lipped mussels 295
Main group Name Occurrence in Occurrence in other NZ hosts Impact in NZ shellfish
P. canaliculus and/or
M. galloprovincialis
Platyhelminthes Tergestia agnostomi Both species Unknown Impact unclear
(Digenea)
Crustacea Pinnotheres sp., Both species Numerous shellfish species No clinical impact observed, but Pinnotheres may
(Decapoda) parasitic crab transfer Nematopsis
Crustacea Lichomolgus uncus Both species Numerous shellfish species No clinical impact observed
(Copepoda)
Crustacea Pseudomyicola spinosus Both species Numerous shellfish species No clinical impact observed
(Copepoda)
Annelida Boccardia spp. and Both species Numerous shellfish species. Borer worms causing shell damage and
(Polychaeta) Polydora spp. unmarketable shellfish; potential intermediate
hosts for Marteilia spp.
(b) Pathogens recorded in mussels and other shellfish hosts overseas but not in NZ
Main group Name Occurrence in mytilids Occurrence in other hosts Distribution Impact
Fungus Steinhausia sp. and M. galloprovincialis Rock oysters, clams, Europe, Asia, Western Potential impact on mussel
Steinhausia-like cockles Australia and the USA’s fecundity
microsporidia Atlantic and Pacific coasts
Protozoa Marteilia refringens Mytilus edulis, European flat oyster Europe and North Africa High mortality in oysters,
Paramyxea M. galloprovincialis Ostrea edulis and mortalities reported in
mussels
Protozoa Haplosporidium spp. Mytilus californianus, Unknown North America and Limited impact reported
M. edulis, Europe
M. galloprovincialis
Crustacea Mytilicola intestinalis Mytilus edulis, Oysters, clams, cockles Europe Limited impact except for
(Copepoda) M. galloprovincialis heavy infestations
Crustacea Mytilicola orientalis Mytilus crassitesta Oysters, clams, cockles North America, Japan Limited impact except for
(Copepoda) (from Inland Sea of Japan), and Europe heavy infestations
M. trossulus, M. gallo-
provincialis, M. california-
nus, M. edulis
Table 1 continued
Aquacult Environ Interact 11: 291– 304, 2019
Therefore, in New Zealand, M. galloprovincialis has
the potential to become a significant reservoir of
mytilid pathogens to which GLMs would be exposed,
given the overlapping distribution of the 2 species and
their co-occurrence on GLM farms. A further compli-
cation in the scenario of pathogen transfer from
Mytilus spp. to GLMs is that hybridisation of local M.
galloprovincialis with Mytilus introduced from the
Northern Hemi sphere could be a risk factor to disease
sus ceptibility (Fuentes et al. 2002). M. edulis × M. gal-
loprovincialis hybrids have already been identified on
New Zealand’s sub- Antarctic Auckland Islands (West -
fall & Gardner 2010).
Understanding the susceptibility of the GLM to ex -
isting or new pathogens and parasites is problematic.
Experimental challenge models (e.g. López San-
martín et al. 2016) may provide a way to explore the
susceptibility of the GLM to certain pathogens affect-
ing host species overseas. For existing disease agents
of the GLM, or those found in other New Zealand
shellfish, stress challenge tests (e.g. temperature or
salinity stress) conducted in a laboratory may provide
an avenue to determine the conditions under which
clinical adverse effects might emerge. However,
there are significant barriers to developing a suitable
broad-spectrum challenge model for exotic disease
agents. First, research with exotic pathogens would
require experiments to be confined to high-level bio-
containment facilities, after approval for importation
under the relevant legislation. In the case of the par-
asite Marteilia refringens, which has been identified
as a potential threat to the GLM (see Table 1b), labo-
ratory experimental findings will not reliably reflect
GLM susceptibility under natural conditions as the
parasite has an indirect life cycle that requires an as
yet unidentified intermediate host (Audemard et al.
2004). Ideally, the GLM needs to be exposed to envi-
ronmental settings where the agent and intermediate
host (where relevant) are present. Such research
would require sending GLM samples overseas, where
it is considered a non-indigenous species, but this
would likely be prevented by regulatory barriers.
Adding to the absence of reliable and realistic ex -
perimental challenge models, the often elusive infor-
mation on pathogen ecology and shellfish disease
epidemiology considerably constrains hazard assess-
ment for disease threats to the GLM.
2.3. Challenges for consequence assessment
Significant production and economic losses in -
curred by disease (e.g. reduced growth, decreased
marketable value or widespread mortalities) are of -
ten mentioned during outbreaks, but there are very
few detailed quantitative assessments (Castinel et al.
2014). The potential consequences of aquatic dis-
eases are as challenging to forecast as their likeli-
hood of occurrence. For example, discovery of Per -
kin sus olseni in farmed GLMs in the South Island of
New Zealand during routine stock health assessment
in 2014 was not unexpected, as this parasite has a
wide host range globally, including New Zealand’s
North Island (Hine & Diggles 2002). Infection with P.
olseni is known to cause mortality in clam and Aus-
tralian cultured greenlip abalone. In this instance,
the discovery of P. olseni in the South Island ap -
peared to be a simple range extension within New
Zealand, with no apparent impact on GLM stocks.
Nonetheless, this situation raises the issue of the
GLM acting as a vector or reservoir for pathogens
causing disease in other shellfish.
Indirect impacts of shellfish disease can be signifi-
cant for the mussel farming industry, even when out-
breaks occur in a different species. For example,
although GLMs are not susceptible to the flat oyster
parasite Bonamia ostreae, they may act as a vector, as
can any shellfish species growing in an infected area
(Culloty & Mulcahy 2007, Mortensen et al. 2007,
Peeler et al. 2011). As such, following an outbreak of
this parasite in farmed flat oysters O. chilensis in
New Zealand in 2015, restrictions on movements of
farmed GLM from infected regions were introduced
to minimise the risk of inadvertent B. ostreae spread
to wild flat oyster fisheries (MPI 2018).
Consequence assessment is made particularly
complex and uncertain by the fluctuations of envi-
ronmental factors that influence host−agent inter -
actions and disease emergence in new hosts or in
new regions. Likewise there is no reason why the
same environmental variations could not also disrupt
parasitic lifecycles and reduce disease incidence.
Disease transmission, pathogenicity and virulence
may be enhanced by changes in environmental
parameters, e.g. sea temperature and salinity (Shee-
han & Power 1999, Groner et al. 2016, Stephens et al.
2016). Warmer seas can modify the behaviour of
pathogenic organisms and their interactions with the
environment, for example by increasing host suscep-
tibility to disease or providing conditions (e.g. nutri-
ent enrichment) favourable to opportunistic agents
(Harvell et al. 1999, Johnson et al. 2010). Though
most significant effects documented to date are for
larval stages, ocean acidification, due to human-
induced increases in atmospheric carbon dioxide,
has already detrimentally affected the composition of
296
Castinel et al.: Disease threats to green-lipped mussels
calcium carbonate shells of mussels and other shell-
fish (Barton et al. 2015, Wahl et al. 2018). There are
already signs that open ocean waters off New
Zealand are acidifying, suggesting that coastal shell-
fish species could become more vulnerable to envi-
ronmental stressors (Capson & Guinotte 2014). How-
ever, in the short to medium term, coastal and
estuarine animal populations are far more likely to be
stressed or impacted by local anthropogenic activi-
ties in adjacent catchments, such as freshwater run-
off or sedimentation from land deforestation (Diggles
2013, Knowles et al. 2014). Those events are already
taking place along New Zealand coasts, which could
contribute to the emergence of opportunistic patho-
gens that undermine the health of wild and cultured
shellfish.
The epidemiology of aquatic diseases is a highly
dynamic field which would greatly benefit from
systematic environmental monitoring studies and
investigations of mortalities, especially in produc-
tion areas. Assuming that there are disease agents
to which GLMs are susceptible, understanding the
generic risk factors that may predispose this
species to disease is highly relevant to consequence
assessment.
3. RISK PATHWAYS FOR THE SPREAD OF
DISEASE AGENTS: NEW ZEALAND CONTEXT
3.1. International risk pathways for exotic agents
Pathways for the introduction and spread of aqua -
tic diseases are poorly understood. Potential mecha-
nisms for the introduction of mussel pathogens and
parasites to New Zealand (and subsequent spread
within the country) are shown in Fig. 2. New Zea -
land’s isolation means that anthropogenic activities
297
Fig. 2. Main types of international risk pathways for mussel pathogens and parasites into New Zealand, and major features of
the domestic network that may interact with aquaculture
Aquacult Environ Interact 11: 291– 304, 2019
provide the most plausible pathways for the initial
incursion of exotic agents (Hewitt & Campbell 2007),
with natural pathways (e.g. ocean currents) expected
to be relatively unimportant. For example, long-
distance transmission of most infectious organisms is
likely curbed by the limited persistence of free-living
microbial particles outside the host (Murray 2013,
Mojica & Brussaard 2014). Nonetheless, migratory
animals such as turtles and seabirds could play a role
in the natural dispersal of pathogens and parasites
(Hayward 1997, Steele et al. 2005, Thieltges et al.
2013). Rafting of floating debris covered with biofoul-
ing was inferred as the most likely scenario for the
trans-Pacific range extension of the flat oyster Ostrea
chilensis from New Zealand to Chile (Foighil et al.
1999), and this potential risk pathway was closely
monitored when debris from the 2011 Japanese
tsunami washed ashore in Hawaii and the northwest-
ern USA (NOAA 2015).
In terms of anthropogenic spread, translocation of
live aquatic animals (or associated equipment) to
support aquaculture growth has been one of the most
significant risk pathways globally (Minchin 2007,
FAO 2012). For example, Bonamia ostreae emerged
as a new parasite causing significant disease out-
breaks in the European flat oyster O. edulis after spat
was introduced from North America to restock native
populations in Europe (Bishop et al. 2006, Peeler et
al. 2011). In New Zealand, the importation of live
shellfish for aquaculture or human consumption is
currently not permitted. Similarly, shellfish products
and equipment used for aquaculture or for other
aquatic activities can only be imported under strict
sanitary and phytosanitary requirements. However,
the volumes of (inadvertently or willingly) un de -
clared goods intercepted at the border during inspec-
tion (MPI 2017) are a reminder that illegal introduc-
tions cannot be ignored as an entry mechanism.
The predominant pathway for the introduction of
new aquatic organisms into New Zealand is likely to
be the ongoing arrivals of international vessels
(Hewitt et al. 2004). A range of vessel types have
been implicated in the inadvertent spread of new
species to New Zealand. These include merchant
ships, cruise ships, fishing vessels, recreational boats
and towed structures such as barges and drilling
platforms (Foster & Willan 1979, Floerl et al. 2005,
Coutts & Forrest 2007, Dodgshun et al. 2007, Hayden
et al. 2009, Hopkins & Forrest 2010a,b). Associated
mechanisms include hull biofouling (Bell et al. 2011),
the discharge of ballast water and associated sedi-
ments (Carlton 1985, Hayward 1997, Taylor et al.
2007) and the transfer of mobile organisms (e.g.
crabs, sea stars) in recesses such as the sea chests of
large vessels (Coutts & Dodgshun 2007, Frey et al.
2014).
Biofouling is undisputed as a significant mecha-
nism for the transfer of bivalves and other macrofoul-
ing organisms across long distances; the introduction
of infected shellfish via this mechanism is the most
likely risk pathway for the transport of new disease
agents to New Zealand. Many of the globally impor-
tant cultured shellfish species that have experienced
disease in a farming environment are also common
biofouling organisms (Minchin & Gollasch 2003,
Hewitt et al. 2009). Studies of vessels arriving in New
Zealand have revealed the presence of Mytilus gal -
loprovincialis, Crassostrea and Ostrea species and
exotic Perna species (Hopkins & Forrest 2010a,c).
Biofouling species may be direct hosts for pathogens
or parasites (e.g. infected oysters or mussels) or may
act as asymptomatic carriers or intermediate hosts
(Tan et al. 2002, Peoples 2013). However, there is
only limited evidence to support the association
between biofouling and disease incursions. A survey
using molecular and histopathology techniques
screened for target pathogens (B. exitiosa, B. ostreae,
Perkinsus marinus, P. olseni, Marteilia refringens,
Haplosporidium nelsoni) in 1500 molluscs sampled
over 3 yr from New Zealand international ports (Gias
& Johnston 2010). No exotic shellfish pathogens were
identified, but pathogens already in New Zealand
such as B. exitiosa and Microsporidium rapuae were
present in biofouling molluscs. Similarly, the role of
ballast water and sediment in transferring microbes
has been demonstrated for human pathogens such as
Vibrio spp. but has yet to be proven for disease
agents of aquatic animals (Ruiz et al. 2000, Drake et
al. 2007).
The recent implementation in New Zealand of a
Craft Risk Management Standard (CRMS) for man-
aging biofouling on international vessel arrivals (MPI
2014) is likely to lead to a major reduction in the
ongoing risk of biofouling. The CRMS promotes best
practice to minimise fouling on submerged surfaces
of vessels arriving in New Zealand. A clean hull is
required, for which the allowable biofouling is con-
strained to goose barnacles and a low coverage of
globally cosmopolitan taxa such as bryozoans and
barnacles. In terms of risk to shellfish aquaculture,
compliance with the CRMS means that a vessel
would not be allowed into New Zealand waters if it
harboured molluscs on its hull. In practice, some
residual risk is almost certain due to fouling by mol-
luscs and other organisms in the niche areas of large
vessels (Coutts & Dodgshun 2007). These include sea
298
Castinel et al.: Disease threats to green-lipped mussels
chests and other hull locations that are prone to foul-
ing, hard to inspect or difficult to effectively treat in-
water (Lewis & Dimas 2007, Growcott et al. 2017).
3.2. Domestic risk pathways
As risks from international pathways cannot be
completely eliminated, there remains the need for an
ongoing focus on internal biosecurity and manage-
ment of domestic borders. Key pathways for the do -
mestic spread of disease agents in New Zealand are
similar to the international ones (Dodgshun et al.
2007) but are more varied in terms of the range of
anthropogenic activities (Fig. 2). Of particular rele-
vance are mussel industry transfers, since GLM spat
and seed are routinely transported between growing
regions (Forrest & Blakemore 2006) with no quaran-
tine period. These movements carry the potential to
transfer disease or disease agents with infected stock
or with entrained biofouling, water or sediments
(Murray 2013). In the event of an infectious disease
incursion in a spat-producing region, the infection
could spread very rapidly throughout the industry,
unless domestic pathway controls were implemented
quickly or were already in place.
Disease spread via stock movements in New Zea -
land was illustrated in 2010 during the first series of
mortality outbreaks in Pacific oysters associated with
the OsHV-1 microvar, in which spat losses of ca. 90%
were recorded (Bingham et al. 2013, Castinel et al.
2015). In most cases, infected stock continued to be
transferred to areas where there were no observed
mortalities (in an attempt to keep stock alive), with
subsequent disease outbreaks in the recipient areas.
Movements of equipment and barges from affected
areas to other parts of the country may have also con-
tributed to the spread of virus, as sharing equipment
between shellfish farms is the second most important
source of risk after movements of infected stock
(Peeler et al. 2007).
Non-industry pathways are also likely to be of sig-
nificance in the domestic spread of disease agents. In
particular, recreational vessels are considered a sig-
nificant risk pathway for the spread of biofouling
organisms and, by association, potentially infectious
agents. Other contributing mechanisms could in -
clude the transport of potentially harmful organisms
in vessel bilge water (Fletcher et al. 2017, Pochon et
al. 2017) and the transfer of recreational equipment
among water bodies (Sinner et al. 2013). Addition-
ally, and by contrast with international transfers, nat-
ural dispersal is likely to be relatively important at
domestic scales. As most aquatic pathogens have a
horizontal transmission (i.e. by contact), dispersal in
the water column (e.g. through tidal currents) is
likely to play a significant role in the local spread of
disease (Whittington et al. 2018), especially in areas
with a high density of farms in close proximity (Mur-
ray 2013, Pernet et al. 2016). Furthermore, since most
shellfish aquaculture operations in New Zealand are
open water systems, it is reasonable to assume that
an organism newly established in wild populations
will eventually spread to adjacent or related farmed
stocks and vice versa (Peeler et al. 2011). The GLM
aquaculture industry is tightly connected, and grow-
ing areas overlap with non-industry activities and
corridors. Additionally, there are still considerable
knowledge gaps and areas of uncertainty with res -
pect to critical points for those risk pathways, which
makes area-wide management of potentially harmful
organisms even more challenging (Table 2).
Development of effective preventative and control
strategies to address pathway risk is therefore prob-
lematic. New Zealand does not yet have any compre-
hensive national action plan to manage domestic
pathways for the spread of potentially harmful aqua -
tic organisms. The aquaculture industry has devel-
oped operational guidelines to encourage best man-
agement practices for biosecurity (AQNZ 2016), for
example to improve reporting procedures for better
traceability of stock movements or to manage risks
from biofouling and entrained water (e.g. bilge
water) or sediments. Yet, in spite of these guidelines,
most aquaculture companies seem reluctant to plan
for and implement proactive risk-reduction measures
(Castinel et al. 2015, Sim-Smith et al. 2016).
4. A WAY FORWARD?
Until 2010, there was a perception that the New
Zealand shellfish aquaculture industry was largely
immune to disease threats. This was based on pre-
sumed resilience to diseases for the 2 main culture
species (GLMs and Pacific oysters) and a view that
New Zealand’s geographic isolation conferred some
level of protection against biosecurity incursions.
However, the emergence of the OsHV-1 microvar
in Pacific oysters in 2010 and Bonamia ostreae in
flat oysters in 2015 with associated important socio-
economic impacts in aquaculture, began to challenge
that perception and has reinforced the need for
better biosecurity practices.
Despite the wake-up calls experienced by Pacific
and flat oyster industry sectors and improved under-
299
Aquacult Environ Interact 11: 291– 304, 2019
standing of potential risks and management opportu-
nities in New Zealand (AQNZ 2016, Georgiades et al.
2016, MPI 2016), the GLM industry remains highly
vulnerable to new incursions or emergence of dis-
eases, and there is little evidence of industry streng -
thening their biosecurity practices. Genomics have
shown that considerable improvements can be made
to control diseases in livestock, and selective breed-
ing has been deemed a key management tool to con-
trol diseases in shellfish (Hollenbeck & Johnston
2018). More scientific evidence is still needed to
demonstrate the net contribution of selective breed-
ing to disease resistance in shellfish. There are also
some caveats to consider, for example the need to
manage inbreeding and ensure that the genetic di -
versity of germplasm is preserved. In addition, the
effectiveness of selective breeding for resistance to
disease varies with its epidemiology and with the
biology of the pathogen or parasite (Bishop & Wool-
liams 2014).
As highlighted in this paper, there is a fundamental
lack of scientific knowledge around aquatic disease
risk to the GLM in the New Zealand context. This
could be stated more broadly for aquaculture species
found in a limited geographic range and/or cultured
in areas where there is little, if any, exposure to
aquatic diseases. This type of baseline information is
essential to the development of effective animal
health strategies and policies, and a new approach is
required to progress risk assessment and manage-
ment of aquatic diseases (Pernet et al. 2016).
Addressing some of the key uncertainties regard-
ing disease threats to farmed mussels in New Zea -
land requires considerable fundamental research
across biological, ecological and social areas. This
would not only help fill critical knowledge gaps, but
also increase confidence in the basis for risk manage-
ment interventions. These considerations are valid
beyond New Zealand borders, and priorities for
future work in aquatic animal health should focus on
improving our understanding of risk factors and our
ability to predict disease outbreaks to prevent them
or at least limit their impacts (Pernet et al. 2016). To
enable better prediction and understanding of host−
environment−disease agent interactions, epidemio-
logical studies will be critical to understand emerg-
ing disease patterns and drivers at the host popula-
tion level (Audemard et al. 2004, Subasinghe 2005,
Engelsma et al. 2010, Peeler et al. 2012, Paul-Pont et
al. 2013). Such studies remain complex for the GLM,
but a start would be to explore conducting research
overseas on suitable surrogate species (e.g. a Perna
species). New Zealand scientists could also collabo-
rate on research projects seeking to elucidate the life
cycle of mussel parasites where disease occurs. This
would help refine New Zealand’s risk assessment for
some exotic mussel parasites. Cost-effective detec-
tion and monitoring tools are also becoming increas-
300
Critical point Contributing factors and related uncertainties
Introduction into NZ • Lack of knowledge on likelihood of agent uptake in source region, transport survival
and release in recipient region (NZ)
• Poor understanding of the role of biofouling, water (e.g. ballast water) and sediments
in vectoring pathogens or parasites
Agent establishment in • Lack of effective tools for detection, eradication and containment of new agent
recipient environment/host • Host range and reservoirs poorly understood, and susceptibility to potential exotic
agents unknown
• Uncertainty regarding pathogen exchange between hosts as well as the identity of
intermediate hosts
Domestic spread of agent • Limited understanding and inherent variability of natural dispersal processes and
to wild or cultured mussels domestic anthropogenic pathway risk
• Absence of or ineffective preventative measures within aquaculture industry or for
other risk pathways
Disease occurrence in wild • Proximity of wild mussels or reservoir hosts to cultured GLM
or cultured mussels • Poor understanding of environmental risk factors (e.g. temperature) and role of on-farm
practices (e.g. stocking density) in triggering disease outbreaks
Spread of disease among • Absence of or ineffective biosecurity controls in production systems (e.g. hatchery or
aquaculture facilities, sites grow-out sites) and processing facilities (and associated wastewater discharge)
or regions • Lack of record-keeping for traceability or movement controls for actual or potential risk
pathways (e.g. equipment, stock transfers)
Table 2. Pathways for introduction and establishment of a new disease agent of green-lipped mussels (GLM) in New Zealand
(NZ): critical steps, contributing factors and related uncertainties
Castinel et al.: Disease threats to green-lipped mussels
ingly needed to collect real-time data on both envi-
ronmental parameters and stock health. Deploying
sentinels at high-risk sites could reduce the time
lapse between incursion and overt signs of diseases
on farms (Rodríguez- Prieto et al. 2015). Sentinels
could include species that are known to be suscepti-
ble hosts to pests or pathogens of mussels overseas.
Innovative surveillance technologies using molecular
diagnostic methods are showing encouraging results
(Gias & Johnston 2010, Pochon et al. 2013), but they
need to be firmly grounded in the basic biology of the
pathogen and its host. Early warning systems are
also needed, including regular systematic surveys of
farmed and wild shellfish populations.
Predictive models for regional-scale disease spread,
based on both anthropogenic pathways and natural
dispersal (e.g. using particle dispersion models, net-
work analysis), will inform the development of area-
based management strategies and identify where
management of aquaculture and other anthropo -
genic risk pathways are likely to have the greatest
impact (Forrest et al. 2009, Salama & Rabe 2013, Per-
net et al. 2016, Samsing et al. 2017). Where uncer-
tainty remains, including when quantifying domestic
risk pathways and prioritising interventions, robust
processes for risk assessment and expert judgement
(e.g. Burgman 2005) should be considered to better
characterise the likelihoods and consequences of the
events that lead to disease outbreaks.
With a changing marine environment and the pro -
spect of new disease threats, it is timely for the
aquaculture industry world-wide to secure its future
and the sustainability of its production by tackling
animal health challenges. In New Zealand, the
GLM farming industry is currently leading the
aquaculture sector in terms of production volumes
and export revenue. It is in good standing to influ-
ence behaviours and perceptions across the coun-
try’s aquaculture companies by improving risk man-
agement policies and decisions to minimise impacts
of disease outbreaks on industry, environment and
people. As part of achieving this outcome, industry
support of multidisciplinary research that integrates
ecological, epidemiological, cultural and socio-
economic data is critical (Pernet et al. 2016). The
development of science-based solutions, however,
requires open communication and collaboration be -
tween industry, the regulators, M
⎯
aori and the wider
community. Most importantly, the accountability for
biosecurity and for aquatic environmental health
must be shared and supported by all parties, which
represents both a challenge and an opportunity for
New Zealand.
Acknowledgements. The authors thank Cara Brosnahan,
Henry Lane and Eugene Georgiades from New Zealand’s
Ministry for Primary Industries for their comments on a draft
manuscript. This research was undertaken under funding
from the New Zealand Ministry of Business, Innovation and
Employment, contract CAW1315 (Enabling, Growing and
Securing New Zealand’s Shellfish Aquaculture Sector).
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304
Editorial responsibility: Brett Dumbauld,
Newport, Oregon, USA
Submitted: October 29, 2018; Accepted: April 24, 2019
Proofs received from author(s): June 21, 2019
