Helminth Parasites in Slippers-Shaped Oyster, Crassostrea
iredalei (Faustino, 1932) (Bivalvia:Ostreoida)
1
Rocelle Leron, *2Venus Bantoto-Kinamot
ABSTRACT
Disease caused by viruses, bacteria and parasitic worms is one of the causes in the
decline of Crassostrea eridalei. Since previous studies mostly focused on microscopic
parasites, this study aimed to identify the helminthic parasites of C. eridalei. Randomly
collected samples from Cambuilao, Bais City Negros Oriental were categorized
according to size, depurated, dissected and examined for the presence of parasites.
Collected parasites were then counted and identified to lowest possible taxon under
the light microscope. Results of this study showed that out of 90 samples examined,
a total of 53 Crassostrea iredalei were found to be infected with parasites. Fifty of
which were infected with annelids with a prevalence of 45 in shell length 1-3cm,
37 in shell length 4-6cm, and 69.5 in shell length 7-10cm. Two were infected
with Platyhelminthes with a prevalence of 5 and 4.16 in shell lengths 1-3cm and
4-6cm, respectively; only one individual was infected with Nemertea with a prevalence
of 4.16. A total of 80 annelid parasites were collected from the infected C. iredalei
individuals with a mean infection intensity ranging from 0.69-2. The annelid parasites
observed in this study were under Class Polychaeta, Families Neridae, Opheliidae,
Hesionidae, Spionidae, Syllidae, Capitellidae, Phyllodocidae, and Polynoidae.
Keywords: Helminth, parasites, Crassostrea, oyster, Bais, Polydora.
INTRODUCTION
Oysters are bivalve mollusks that are
classified under Phylum Mollusca, Class Bivalvia,
Order Ostreoida, FamilyOstredei. Oysters are
widely distributed and found in habitats like
lagoons, estuaries, and brackish water in both
temperate and tropical regions (Angell, 1986;
Raj, 2008). They are considered as one of
the foundation species which help maintain
biodiversity, population, and food web dynamics,
nutrient cycling, and water quality (Raj, 2008).
There are three known genera of oysters: Ostrea,
Sacosstrea, and Crassostrea (Angell, 1986).
The Crassostrea variety is considered as the
most important commercial species of oysters
1 ,2
College of Arts and Sciences, Biology Department Negros Oriental State University
Main Campus I, Kagawasan Avenue, Dumaguete City, 6200, Philippines
*[email protected]
found throughout Southeast Asia (Angell, 1986).
In the Philippines, Crassostrea iredalei is one of
the four species cultivated along with Crassostrea
cucullata, C. malabonensis, and C. palmipes.
Of these four species, C. iredalei is the most
commercially wanted because it grows at a faster
rate to a larger size and has straight shell margins
which make them easier to open (Food and
Agriculture Organization of the United Nations,
2016).
According to Robledo et al. (2014), the
population of Crassostrea iredalei suffers a
significant decline due to overharvesting,
environmental pollution or diseases. Disease
of bivalve mollusks is mostly caused by
biological agents such as viruses, bacteria, fungi,
Prism, Volume 20 Issue 2, (July.- Dec. 2015)
40
protists, digenean trematodes, polychaetes
and copepods (Boehs et al., 2010). Niajah
et al. (2008) reported that sampled oysters
from Setiu Wetland, East Coast Peninsular
Malaysia, harbor Shewanellaputrifaciens, Vibrio
parahaemolyticus, Vibrio vulnificus, Vibrio
cholerae, Enterobacter cloacae, Escherichiacoli
as well as Chromobacteriumviolaceum bacteria.
A protozoan parasite, Nematosis sp. was found
to infect C. iredalei in Palau Bentong, West Coat
of Penang Malaysia. The same species, together
with the cestode parasite, Tyloceplahumsp,
was also found to infect C. iredalei in Ivisan,
Capiz, Philippines (Ezaro et al., 2010). These
protozoan parasites were also observed
to infect other species of Crassostrea. The
Haplosporidiumnelsoni, another protozoan
parasite, causes the Multinucleated SphereX or
MSX disease which affects mollusks; the MSX first
appeared in 1957 at the Delaware Bay (Ewart&
Ford, 1993). Other protozoan parasites like the
Perkinususmarinus, have caused problematic
oyster disease particularly in Crassostrea virginica
varieties in Georga, USA (Power et al.,2006). A
protist, Marteiliasyndeyi, causes a QX disease that
is described by Dang et al. (2013) to decrease
meat quality, reproductive capacity and massive
mortalities in Crassostrea viginica.
Though Crassostrea has been subject to
many parasite related studies, (Boehs et al.,2010;
Dang et al.,2013; 2005 De Vera et al.,2005; Ezaro
et al.,2010), most of these focused on microscopic
parasites such as bacteria, protozoans, and
ciliates. Knowledge about the helminth parasites
of oysters and its impact on Crassostrea ireladei
culture in the Philippines is still scarce.
This study aimed to identify the helminth
parasites found in Crassostrea iredalei and
determine the parasitic load in terms of prevalence
and intensity. Results of this study will serve as
the basis for identifying the macroscopic parasites
of the Crassostrea iredalei and therefore will
Helminth Parasites in Slippers-Shaped Oyster
help in improving the meat quality, reproductive
capacity, marketability, and production of farmed
Crassostrea iredalei.
MATERIALS AND METHODS
Collection of Crassostrea iredalei Samples
Crassostrea iredalei (Faustino, 1932) or
slipper-shaped oyster is a bivalve mollusk that
can be distinguished by the presence of a black
scar in its adductor muscle (Figure 1). A total
of 90 samples were randomly collected from
Cambuilao, Bais City, Negros Oriental. The
samples were then slightly washed, placed in an
icebox and transported to the Biology Laboratory,
Negros Oriental State University. In the laboratory,
each bivalve sample was measured for its length
and height using a Vernier caliper and was sorted
out by size. Each sample was placed in individual
containers with seawater from the actual site of
collection. After which, the bivalves were allowed
to depurate for 3-4 days. Depuration is a process
by which shellfish are put in tanks of clean
seawater under conditions which maximize the
natural filtering activity which outcomes in the
expulsion of intestinal contents, which enhances
separation of the expelled contaminants from
the bivalves, and prevents their recontamination
(Ronald et al., 2008). In this study, plastic
containers were used as an alternative for tanks to
contain both oysters and seawater, and to capture
any impurities including parasites as the oysters
depurate. Each oyster sample was individually
dissected using dissecting sets for helminth
parasite examination. Depurated water was also
examined for the presence of parasite.
41
Leron, and Kinamot
Figure 1. Crassostrea iredaleicolleted from Cambuilao, Bais, Negros Oriental. (BS=black scar),
(AM=adductor muscle), (MN=mantle), (CS=cup shaped shell).
Collection and Identification of Helminth
Parasites
Taxonomy Assessment, Mississippi.
The method described by Gardner et al.
(2012) was adapted and modified for parasite
collection. Helminth parasites were collected
from the oysters’ mantle and depurated water.
Collected parasites were sorted out into lowest
possible taxon, counted and placed in plastic vials
with labels and containing 70% ethanol solution
for storage.
The parasites were identified under the
compound microscope using the guides of
Handley (1999; 2000); SAORC, 2003; Rodrigo
(2006); Martin et al. (2012); Cinar et al. (2015)
and online databases http://www.annelida.net/,
http://species-identification.org/, and http://www.
marinespecies.org/. Identified parasites were
then verified by MelihCinar, Ph.D., a Marine
Biology professor at Ege University, Izmir, Turkey,
who specializes in taxonomy and ecology of
polychaetes. The same samples were verified by
Jerry A. McLelland, Ph.D., from Gulf Benthic
Data Analysis
The method used by Mergo& Crites (1986)
was adopted for the determination of parasitic
prevalence and the mean intensity of the shell
length of the slipper-shaped oyster. Prevalence
is the proportion of infected hosts among all the
hosts examined while infection intensity is the
total number of parasites found in each host.
RESULTS
In this study, the shell length of Crassostrea
iredalei was ranged from two to ten cms. Out of
90 samples examined, a total of 53 Crassostrea
iredalei were found infected with helminth
parasites; and almost all infected samples were
found with blisters from the periostracum to the
nacreous layer of the shell (Figure 2). Fifty out
of 53 infected samples harbored annelids with
42
a prevalence of 45% in shell length 1-3cm, 37%
in shell length 4-6cm, and 69.5% in shell length
7-10cm. Two were infected with Platyhelminthes
with a prevalence of 5% and 4.16% in shell lengths
of 1-3cm and 4-6cm, respectively. There was only
one individual infected with Nemertea with a
prevalence of 4.16% (Table 1).
Helminth Parasites in Slippers-Shaped Oyster
A total of 80 annelid parasites were collected
from the infected C. iredalei individuals: two
Platyhelminthes parasite and one nemertean
parasite. Data shows that the annelids bear the
highest infection intensity with a mean intensity
ranging from 0.69-2 (Table 2).
Table 1. The number of infected individuals and prevalence of helminth parasites in each size range
of Crassostrea iridalei
Shell
No.
Number of Infected C. iredalei
Prevalence (%)
Length Examined Annelida Platyhelminthes Nemertea Annelida Platyhelminthes Nemertea
(cm)
1-3
20
9
1
0
45
5
0
4-6
24
9
1
1
37
4.16
4.16
7 - 10
46
32
0
0
69.5
0
0
Total
90
50
2
1
Table 2. Mean infection intensity of helminth parasites in Crassostrea iredalei
Shell
No. of Parasites collected
Mean Intensity
Length
Annelida Platyhelminthes Nemertea Annelida Platyhelminthes Nemertea
(cm)
1-3
15
1
0
1.67
1
0
4-6
18
1
1
2
1
1
7-10
47
0
0
0.69
0
0
Total
90
2
1
Figure 2. Blisters and parasites found in the shell of Crassostrea iredalei. (BL=blister) (P=parasite).
Leron, and Kinamot
The annelid parasites observed in this
research were under Class Polychaeta, Families
Neridae, Opheliidae, Hesionidae, Spionidae,
Syllidae, Capitellidae, Phyllodocidae, and
Polynoidae (Figure 3).
Family Nereididae is distinguished by the
presence of rectangular to a triangular head. A
pair of short antennae between a pair of jointed
palps with stout bases is also present followed or
surrounded by four pairs of long tentacular cirri
(Read, 2004). Two pairs of large eyes are also
observed (Figure 3A).
Members of Family Opheliidae sand
burrowers; they are short-bodied, cigar-shaped,
and muscular. Their head is sharply conical,
sometimes with a knobbed tip and its mouth
is just a ventral slit (Figure 3B). Opheliids are
also considered as deposit feeders, but they are
probably selective in their intake of particulate
material. Adult species measures up to 20 mm in
length and slender, while other species are more
desirable and maggot-like and may reach up to 30
mm long (Read, 2004).
Hesionidaepolychaetes have prostomium
that is simple or bilobed containing four eyes,
two to three antennae and two palps that are each
divided into two sections (Allen, 1904). Its first
segment dorsally reduced and with up to eight
pairs of tentacular cirri present on cephalized
segments. Its pygidium is with two cirri (Figure
3C).
Family Spionidae is generally small and
slender active worms, with head palps used for
feeding. Their palps arise dorsally on either
side of a narrow prostomium. Spionidpygidial
structures are varied and include short cirri (one
to three pairs or many), lobes, cups, and plates
(Figure 3D). Adult size ranges from 150 mm long
and 10 mm diameter, but more usually 10-30 mm
(Read,2004).
Syllids are typically of small size and delicate
in appearance; they are characterized by having
43
forms with long thin antennae and noticeable
dorsal cirri that stand partly upright from the body
and could be annulated. Their prostomium has
three antennae: the median one is the posteriormost; a pair of palps directed somewhat ventrally,
and with one or two pairs of eyes present. A
proventriculus or a gizzard-like structure is
present, which is usually visible through the body
wall. One or two pairs of tentacular cirri are
possessed by its peristomium (Figure 3E). Adult
size is around 20 mm or less in length (Read,
2004).
Members of Family Capitellidae are threadlike deposit dwellers that live in unlined, rambling
burrows and are considered to be relatively nonselective particle feeders. Capitellid worms are
long, delicate, and difficult to collect intact. The
prostomium is conical to pointed, and the first
segment usually lacks chaetae (Figure 3F). Adult
size reaches up to 50 mm long, and is very thin
(Read, 2004).
The Phyllodocids are long, slender, and
very active carnivorous worms characteristically
possessing enlarged dorsal and ventral cirri
which are often flattened and leaf-like and is
characteristically colourful family of polychates
(Read,2004). The anterior of their head is often
somewhat shovel-shaped and bears a group of four
'antennae' (the ventral pair is probably modified
palps). Further back, a fifth median antenna may
be present (Plate 3G). Jaws are absent, but with
an anterior gut that has a very long eversible
proboscis which is usually papillose and with
terminal papillae; 2-4 pairs of tentacular cirri on
2-3 variably-fused segments behind the head are
also observable (Read,2004). Adult size members
of this family are less than 20 mm long.
Polynoidae scale worms are dorsoventrally
flattened, often rather oval-shaped. Their upper
surface is typically fully protected by a number of
large overlapping plates, known as elytra, each of
which may be adorned and fringed with papillae,
44
tubercles, and hairs (Figure 3H). Located near
its center is the mushroom-like attachment point
of each elytron. Adult size is up to 100 mm long
(Read, 2004).
Helminths under Phylum Nemertea were
distinguished by the presence of retractable
Helminth Parasites in Slippers-Shaped Oyster
proboscis, a long muscular tube that is thrust
out swiftly when grasping their prey (Figure
3I). Platyhelminthes on the other hand,
have dorsoventrally flattened and bilaterally
symmetrical body (Figure 3J) (Hickman et al.,
2008).
Figure 3. Images of parasites identified from Crassostrea iredaleiunder LPO (100X) A.Nereididae
B.Opheliidae. C. HessionidaeD. SpionidaeE. Syllidae F. CapitellidaeG. PhyllodocidaeH. PolynoidaeI. Nemertean J. Platyhelminthes.
Leron, and Kinamot
DISCUSSION
Annelids are helminths that are less known
to be parasitic; however, there are cases that
involve polychaete infection (Handley et al., 2003;
Struck, 2008) which affected the physiological
condition and marketability of their host. For
instance, the presence of polychaete in Saccostrea
commercialis affected its marketability in Australia
(Skeel, 1979). In Hawaii, another polychaete,
the Boccardiaproboscidea, was found to heavily
infect the oysters (Bailey-Brock, 2000). These
polychaetes affect cultured mollusks, including
oysters by reducing their flesh condition through
delayed growth rates and thus increasing mortality
(Simon et al., 2009). In New Zealand, polychaete
under the genus Polydora has been reported to
damage commercially important bivalves such
as the Crassostrea gigas, Perna canaliculus, and
Pectennovazelandiae (Read, 2010). In this study,
it was found out that Crassostrea iredalei is also
susceptible to annelid infection. Out of 90 annelid
parasites identified, polychaete specifically under
the genus Polydora was observed to infect most
of the oyster individuals. According to Lleonart
et al. (2003), Polydora is known to be a parasitic
polychaete that infects mollusks such as abalones
and oysters. This species usually burrows into a
substrate that contains calcium carbonate such as
the shells of oysters found in muddy sediments
(Hill, 2007).
Boring polydorids have frequently been
considered as parasitic organisms from an
anthropogenic rather than ecological point of
view (Martin &Britayev, 1998). As soon as they
infest species of mollusks such as oysters that
are cultivated or harvested as a fishery resource,
they are immediately regarded as pests (Martin
&Britayev, 1998). It was also reported in 1979
that four polydorid parasites caused serious
damage to cultured bivalves in Australia, including
Crassostrea iredalei, by creating irritating and
45
often fatal mud blisters between the shell and
mantle (Skeel, 1979). The polydorid parasite
has also been alarming to Australia and Chile for
heavily infecting the farmed oysters (Handley,
2003; Moreno,2006).
Polydora species infect oysters in two
ways - either boring through the shell from the
outside using metabolic acids (Haigler, 1969;
Hadley, 1998) or by entering the oyster’s mantle
cavity as a larva and thus setting within the oyster
(Skeel,1977; Handley,1998). When parasites
reach the inner nacreous layer, the oyster reacts
to the irritant and secretes a layer of conchiolin
at the site of contact with mantle tissue, forming
a “mud blister”(Angell,1986). It is notable in
this study that most of the oysters showed mud
blisters in their shell. These observations could
support that these mud blisters were the results of
the oyster’s reaction to the irritant caused by the
parasites. Mud blister influences the physiology
of the oysters which would further increase the
susceptibility of oysters to parasitism.
Moreover, results showed that the size of
oysters may affect its susceptibility to parasites.
Parasite prevalence increased in parallel with
the increase in oysters shell length (Table 1.)
A similar trend is found in the study of Martin
and Britayev (1998). Oysters with larger size are
more or less older and so have been exposed to
planktonic larvae settlement or adult migration
of parasites for a longer period than small sizedoysters. In addition, large oysters provide more
space for parasites than small oysters (Martin
&Britayev, 1998). Moreover, the susceptibility of
Crassostrea iridalei to polychaete parasites could
also be due to the physiological stress induced
by the environmental conditions. According to
several studies, susceptibility to parasitism and
associated disease may increase when a host
suffers from physiological stress that is brought
about by extreme environmental conditions
(Chapin 1991; Gustaffson et al. 1994; Urawa
46
Helminth Parasites in Slippers-Shaped Oyster
1995; Lenihan et al., 1999). Stressors may include
flow speed over the oysters’ reef, oxygen stress,
temperature and salinity variation and poor food
quality (Paynter and Burreson 1991; Burreson
and Calvo 1996; Chu 1996; Lenihan et al. 1999).
Oysters in low flow and reduced food quality are
in poorer physiological condition and less likely
to fight off parasitic infection than oysters in high
flow. For example, it was found out that oysters
exposed to higher levels of salinity and hypoxia
showed greater susceptibility to parasite such as
Perkinusmarinus (Lenihan et al., 1999).
Fortunately, the occurrence of parasites
in C. ireadalei is not threatening and does not
pose serious health risk for human consumption
because they are not zoonotic. According to
Brown (2012), polychaetes specifically Polydora
are sensitive to salinity and temperature. They
grow well at higher temperatures rather than
lower temperatures. Also, they cannot tolerate
extremely low salinity; thus, exposing it to low
salinity and cold water would initiate its death.
Furthermore, if oysters infected with parasites
are accidentally eaten, the acidic environment
in the stomach of humans could result in the
parasite's death. Though this implies that oyster
parasites do not impose threat in public health,
these parasites should still be carefully studied as
well as its eradiation from its hosts due to massive
destruction that it could cause to oysters which
could result in the decline of oysters supply.
under genus Polydora of the Family Spionidae
was observed to greatly infect C. iredalei. The
mean infection intensity of annelid in all infected
individuals ranged from 0.69-2. Oysters with
larger size and shell length harbored more
parasites that the small ones.
CONCLUSION
Allen, E. J. (1904). The anatomy of Poecilochaetus,
Claparède.
Quarterly
Journal
of
Microscopical Science, 48, 79-151.
The helminthic parasites that infect C.
iredalei were found to be annelids, nemerteans,
and platyhelminthes. Most of the individuals were
infected with annelids with a prevalence ranging
from 37%-69.5%. The annelids were under
Class Polychaeta, under the families Neridae,
Hesionidae, Syllidae, Spionidae, Phyllodocidae,
Opheliidae, Capitellidae, and Polynoidae. Species
RECOMMENDATIONS
This study recommends investigating
the effects of these helminth organisms to the
physiology of Crassostrea iredalei. Future studies
regarding the factors which increase the risks of
parasitism in C. iridalei are also suggested. Parasitic
prevalence should be observed in different age
groups. Lastly, symbiotic relationship of these
helminths and the oyster should also be studied.
ACKNOWLEDGMENTS
The authors would like to express their
heartfelt gratitude to Dr. MelihCinar of Ege
University, Izmir, Turkey and Dr. Jerry A. McLelland
of Gulf Benthic Taxonomy Assessment, Mississippi
for verifying the identification of the helminth
parasites in the Crassostrea iredalei. Likewise,
the authors would like to express appreciation to
the Biology Department of Negros Oriental State
University and SEAFDEC for the logistic support.
REFERENCES
Angell, C. L. (1986). The Biology and Culture of
Tropical Oysters. International Center for
Living Aquatic Resources Management
Studies and Reviews, 13.
Bailey-Brock, J. H. (2000). A new record of the
Leron, and Kinamot
polychaete Boccardiaproboscidea (Family
Spionidae), imported to Hawai’i with oysters.
Pacific Science, 54(1), 27-30. doi:10125/1595
Boehs, G., Villalba, A., Ceuta, L. O., & Luz, J. R.
(2010). Parasites of three commercially
exploited bivalve mollusc species of
the estuarine region of the Cachoeira
River (Ilhéus, Bahia, Brazil). Journal of
Invertebrate Pathology, 103(1), 43–47.
Breitburg, D. L. (1992). Episodic hypoxia
in Chesapeake Bay: Interacting effects
of recruitment, behavior, and physical
disturbance. Ecological Monographs, 62(4)
525–546.doi:10.2307/2937315
Brown, S. W. (2012). Salinity tolerance of the
oyster
mudwormPolydorawebsteri.
Retrieved from http://digitalcommons.
librar y.umaine.edu/cgi/viewcontent.
cgi?article=1040&context=honors
Burreson, E. M., & Calvo, L. M. R. (1996).
Epizootiology of Perkinsusmarinus disease
of oysters in Chesapeake Bay, with emphasis
on data since 1985. Oceanographic
Literature Review, 12(43), 1265.
Chapin III, F. S., Mooney, H. A., Winner, W. E., &
Pell, E. J. (1991). Effects of multiple
environmental stresses on nutrient
availability and use. Response of Plants
to Multiple Stresses. Academic Press, San
Diego, 67–88.
Chu, F-L. E. (1996). Laboratory investigations
of susceptibility, infectivity and transmission
of Perkinsusmarinusin oysters. Journal of
Shellfish Research, 15(1), 57–66.
Çinar, M. E., Dağli, E., Çağlar, S., & Albayrak, S.
47
(2015). Polychaetes from the northern part
of the Sea of Marmara with the description
of a new species of Polydora (Annelida:
Polychaeta: Spionidae). Mediterranean
Marine Science, 16(3), 524–532. doi: 524532
Dang, C., Cribb, T. H., Cutmore, S. C., Chan, J.,
Hénault, O., & Barnes, A. C. (2013). Parasites
of QX-resistant and wild-type Sydney rock
oysters (Saccostrea glomerata) in Moreton
Bay, SE Queensland, Australia: Diversity
and host response. Journal of Invertebrate
Pathology, 112(3), 273–277. doi: 0022-2011
De Vera, A. Z., Mcgladdery, S. E., Humera, A.,
Stephenson, M. F., Mailet, M., &Bourgue, D.
(2005). Occurrence of hemic neoplasia in
slipper oyster, Crassostrea iredalei (Faustino
1928) in Dagupan City, Philippines. Disease
in Asian Aquaculture V, 321-325.
Erazo-Pagador, G. (2010). A parasitological
survey of slipper-cupped oysters (Crassostrea
iredalei, Faustino, 1932) in the Philippines.
Journal of Shellfish Research, 29(1), 177–
179. doi:10.2983/035.029.0111
Ewart, J. W., & Ford, S. E. (1993). History and
impact of MSX and Dermo diseases on oyster
stocks in the northeast region. Northeastern
Regional Aquaculture Center, University of
Massachusetts Dartmouth. Retrieved from
http://web2.uconn.edu/ seagrant/whatwedo/
aquaculture/pdf/nrac200_histdisease.pdf
Fernández Robledo, J. A., Vasta, G. R., & Record,
N. R. (2014). Protozoan Parasites of Bivalve
Molluscs: Literature Follows Culture. PLoS
ONE 9(6): e100872. doi:10.1371/journal.
pone.0100872
48
GanapathiNaik, M., & Gowda, G. (2015).
Assessment of rate of oyster spat fall: A
review. International Journal of Advanced
Scientific and Technical Research, 5(3).
Gustafsson, L., Nordling, D., Andersson, M.
S., Sheldon, B. C., &Qvarnström, A. (1994).
Infectious disease, reproductive effort
and the cost of reproduction in birds.
Philosophical Transactions of the Royal
Society of London: Series B, (346), 1655–
1658. doi: 10.1098/rstb.1994.0149
Haigler, S. A. (1969). Boring mechanism of
Polydorawebsteri inhabiting Crassostrea
virginica. American Zoologist, 9(3), 821–
828. http://dx.doi.org/10.1093/icb/ 9.3.821
Handley, S., & The South Australian Oyster
Research Council and Seafood Services
Australia. (2003). Identification of natural
mudworm species in South Australian
Pacific oyster Crassostrea gigas stocks.
Ascot, Queensland:
Seafood Services
Australia.
Handley, S. J. (1995). Spionidpolychaetes in
Pacific oysters, Crassostrea gigas(Thunberg)
from Admiralty Bay, Marlborough Sounds,
New Zealand. New Zealand Journal of
Marine and Freshwater Research, 29(3),
305–309.doi:10.1080/00288330.1995.9516
665
Handley, S. J. (1998). Power to the oyster: Do
spionid-induced shell blisters affect
condition in subtidal oysters? Journal of
Shellfish Research, 17(4), 1093–1100.
Hill, J. M. (2007). A bristleworm (Polydoraciliata).
Marine Life Information Network. Retrieved
from:
http://www.marlin.ac.uk/species/
Helminth Parasites in Slippers-Shaped Oyster
detail/1410
Lee, R., Lovatelli, A., & Ababouch, L. (2008).
ivalve depuration: fundamental and practical
aspects. Food and Agriculture Organization
(FAO) Fisheries Technical Paper, 511, 139.
Lenihan, H. S. (1999). Physical-biological coupling
on oyster reefs: how habitat structure
influences
individual
performance.
Ecological Monographs, 69(3), 251–275.
doi:10.2307/2657157
Lleonart, M., Handlinger, J., & Powell, M. (2003).
Spionidmudworm infestation of farmed
abalone (Haliotis spp.). Aquaculture,
221(1-4), 85–96. doi:10.1016/ S00448486(03)00116-9
Martin, D., &Britayev, T. A. (1998). Symbiotic
Polychaetes: Review of known species.
Oceanography and Marine Biology: Annual
Review, 36, 217-340.
Moreno, R. A., Neill, P. E., &Rozbaczylo, N. (2006).
Native and non-indigenous boring
polychaetes in Chile: A threat to native and
commercial mollusc species. RevistaChilena
de Historia Natural, 79(2), 263–278.
Niajah, M., Nadirah, M., Lee, K. L., Lee, S. W.,
Wendy, W., Ruhil, H. H., &Nurul F. A. (2008).
Bacteria flora and heavy metals in cultivated
oysters Crassostrea iredalei of Setiu Wetland,
East Coast Peninsular Malaysia. Veterinary
Research Communications, 32(5), 377-381.
doi: 10.1007/s11259-008-9045-y
Paynter, K. T. (1996). The effects
of
Perkinsusmarinus infection on physiological
processes in the eastern oyster, Crassostrea
virginica. Journal of Shellfish Research,
Leron, and Kinamot
15(1), 119–126.
Power, A., McCrickard, B., Mitchell, M., Covington,
E., Sweeney-Reeves, M., Payne, K., & Walker,
R. (2006). Perkinsusmarinus in coastal
Georgia, USA, following a prolonged
drought. Diseases of Aquatic Organisms,73,
151–158. doi: 10.3354/ dao073151
Read, G. B. (compiler) (2004). Review from Guide
to New Zealand Shore Polychaetes.
Retrieved from http://biocollections.org/
pub/worms/nz/Polychaeta/ShorePoly/
NZShorePolychaeta_begin.htm
Read, G. B. (2010). Comparison and history of
Polydorawebsteri and P. haswelli (Polychaeta:
Spionidae) as mud-blister worms in New
Zealand shellfish. New Zealand Journal of
Marine and Freshwater Research, 44(2),
83–100. doi:10.1080/00288330.2010.48296
9
Sanjeeva Raj, P. J. (2008). Oysters in a new
classification of keystone species. Resonance,
13(7), 648–654. doi:10.1007/s12045-0080071-4
Simon, C. A., Thornhill, D. J., Oyarzun, F., &
Halanych, K. M. (2009). Genetic similarity
between Boccardiaproboscidea from
Western North America and cultured
abalone, Haliotismidae, in South Africa.
Aquaculture, 294(1-2), 18–24. doI:10.1016/j.
aquaculture.2009.05.022
Skeel, M. E. (1979). Shell-boring worms
(spionidae:polychaeta) infecting cultivated
bivalve molluscs in Australia. World
Aquaculture Society, 10(1-4), 529-533.
doi:10.1111/j.1749-7345.1979.tb00048.x
49
Sousa, W. P., & Gleason, M. (1989). Does
parasitic infection compromise host survival
under extreme environmental conditions?
The case for Cerithideacalifornica
(Gastropoda: Prosobranchia). Oecologia,
80(4), 456–464. doi:10.1007/BF00380066
Sousa, W. P., &Grosholz, E. D. (1991). The
influence of habitat structure on the
transmission
of
parasites.Habitat
structure(pp.
300–324).Netherlands:
Springer.
doi:10.1007/978-94-011-30769_15
Urawa, S. (1995). Effects of rearing conditions
on growth and mortality of juvenile chum
salmon (Oncorhynchus keta) infected with
Ichthyobodonecator. Canadian Journal
of Fisheries and Aquatic Sciences, 52(S1),
18–23.