predation by neogastropods on turbo cornutus juveniles and other small gastropods inhabiting...
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ORIGINAL ARTICLE Biology
Predation by neogastropods on Turbo cornutus juveniles and othersmall gastropods inhabiting coralline algal turfs
Jun Hayakawa • Tomohiko Kawamura • Satoshi Ohashi •
Naoya Ohtsuchi • Hiroaki Kurogi • Yoshiro Watanabe
Received: 11 October 2011 / Accepted: 28 December 2011 / Published online: 1 February 2012
� The Japanese Society of Fisheries Science 2012
Abstract To understand the effects of predation by
gastropods on juveniles of the Japanese spiny turban snail
Turbo cornutus, a field survey and laboratory experiments
were conducted. The species compositions of the order
Neogastropoda inside turfs of articulated coralline algae
(ACA) on the east coast of Sagami Bay were surveyed
monthly, and the dominant species inside the ACA turfs
were identified. Laboratory experiments were conducted
to examine the effects of predation by the dominant
neogastropods on small gastropods in ACA turfs. Turban
snails, which inhabit ACA turfs during their juvenile
stages, were predated by two muricid gastropods,
Ergalatax contractus and Thais bronni, with the preda-
tion rate of E. contractus being significantly higher than
that of T. bronni. While E. contractus could also predate
two other species of gastropods, Anachis misera and
Cantharidus japonicus, the predation rates on these two
snails were significantly lower than on T. cornutus. The
observed defensive behaviors were different among the
three prey species, and the defensive strategy related to
the calcified operculum of T. cornutus was not efficient
against predation by E. contractus. It is concluded that
the predation by E. contractus represents an important
factor in the mortality of juvenile turban snails inside
ACA turfs.
Keywords Coralline turf � Defense mechanism �Ergalatax contractus � Predation � Turbo cornutus
Introduction
Many benthic marine animals on rocky shores exhibit
strong relationships with specific algal communities [1–3].
Various factors related to these algal communities, such as
food abundance, the physical environment, and the exis-
tence of competitors, strongly influence the survival and
growth of the benthos living within them. The existence of
predators is one of the most important factors affecting the
survival of benthic animals associated with the algal
communities [4, 5].
Algal turfs of articulated coralline algae (Corallinales,
Rhodophyta) are a common type of algal community on
rocky shores in the temperate zone. As articulated coral-
line algal (ACA) turfs are composed of dense solid algal
fronds, the small benthic animals found within these turfs
are thought to be largely protected from physical and
biological disturbances, so ACA turfs contain highly
diverse invertebrate populations [6, 7]. The Japanese
spiny turban snail Turbo cornutus is one of the most
important fishery resources in coastal areas of Japan, and
this species selectively uses ACA turfs as a nursery for
approximately 1 year following settlement of planktonic
larvae [8]. ACA fronds appear to protect turban snail
juveniles from large predators, such as starfish and fish.
However, gastropods belonging to the order Neogastro-
poda found at high densities inside ACA turfs are
potential predators for turban snail juveniles, as shells of
J. Hayakawa (&) � H. Kurogi
Arasaki Marine Biological Station, National Research Institute
of Aquaculture, Fisheries Research Agency, Yokosuka,
Kanagawa 238-0316, Japan
e-mail: [email protected]
T. Kawamura � N. Ohtsuchi � Y. Watanabe
Atmosphere and Ocean Research Institute, The University
of Tokyo, Kashiwa, Chiba 277-8564, Japan
S. Ohashi
Nagasaki Prefectural Institute of Fisheries,
Nagasaki, Nagasaki 1551-4, Japan
123
Fish Sci (2012) 78:309–325
DOI 10.1007/s12562-012-0467-7
T. cornutus juveniles with a drilled hole were collected in
previous field samplings [9, 10].
Despite this hypothesis, however, the feeding habits of
the small neogastropods inside ACA turfs are still largely
unknown, although they are usually considered scavenging
or predatory species. In addition, studies on the density and
species composition of the macrofauna inhabiting ACA
turfs, including neogastropods, have been very limited,
especially in the temperate zone of the Northern Hemi-
sphere [11].
Ergalatax contractus is a common muricid gastropod on
rocky shores in Japanese coastal waters that inhabits vari-
ous algal communities, including ACA turfs. While this
species has been considered a scavenger and opportunistic
predator with a low positivity of attacking [12, 13], it has
been suggested to be a potential predator for abalone
juveniles based on stable isotope analyses conducted in the
same area as the present study [14]. Thus, E. contractus
may be a predator for small gastropods, including T. cor-
nutus juveniles within ACA turfs.
In the present study, the abundance and species compo-
sition of neogastropods inhabiting ACA turfs were moni-
tored monthly on a rocky shore at Nagai in Sagami Bay,
Japan. The predation on T. cornutus juveniles by dominant
neogastropods within ACA turfs, including E. contractus,
was also studied in laboratory experiments. The predatory
behaviors of the neogastropods and the defensive reactions
of several gastropod species, including T. cornutus, were
observed in the laboratory. In addition, shells of dead
T. cornutus were collected from natural ACA turfs at Nagai,
and the percentages of shells with a hole drilled by preda-
tory gastropods were determined. Based on the results of the
field samplings and laboratory experiments, the effects of
predation by sympatric predatory gastropods on the survival
of T. cornutus juveniles are discussed.
Materials and methods
Field survey
From December 2007 to January 2011, field samplings were
carried out monthly to investigate the species composition
and density of neogastropods inside ACA turfs at Nagai
(35�11.500N, 139�35.590E) on the east coast of Sagami Bay,
Kanagawa, Japan. Three quadrates (25 cm 9 25 cm) were
haphazardly set on ACA turfs in the subtidal zone by
SCUBA. The animals, algae, and sand inside each quadrat
were detached and collected using an airlift sampler (suc-
tion dredge) into a 200 lm mesh bag attached to the sam-
pler. Mesh bags containing the samples were immediately
taken to the laboratory of Arasaki Marine Biological Station
(AMBS), which is located close to the sampling area, and
soaked in 25% ethanol–seawater solution for 15 min to
immobilize the collected invertebrates. After soaking, the
samples were separated into two size groups using a 3 mm
mesh sieve, and the gastropods that remained on the sieve
were fixed in a 5% formalin–seawater solution. Identifica-
tion of neogastropod species was performed based on a list
of gastropods inhabiting ACA turfs in the sampling area
[15]. The wet weights of the neogastropods were also
measured from October 2009 to January 2011. The shell
height (SH) of E. contractus was measured using calipers to
a precision of 0.1 mm.
Dead shells of T. cornutus, meaning a shell or part of
shell from which the original architect had disappeared
[16], were sorted from samples both [3 and \3 mm in
size. The size and condition (with/without a drilled hole or
break) of the dead shells were recorded. The sizes of early
juvenile turban snails (i.e., individuals less than 3.5 mm in
SH) were measured in terms of the shell diameter.
Laboratory observations and experiments
General conditions of the experiments
Neogastropods, which were identified as the dominant
species inside the ACA turfs based on the results of the
field samplings, were collected from the subtidal zone at
the sampling site. They were maintained in a water tank at
AMBS until they were used for laboratory experiments.
These gastropods were employed in all subsequent exper-
iments after a starvation period of 2 days.
The general conditions of the experiments performed in
this study are shown in Table 1. All laboratory experiments
were carried out at AMBS with the exception of Experi-
ments 4 and 5, which were conducted at the Nagasaki
Prefectural Institute of Fisheries (NFI; Nagasaki, Japan).
The T. cornutus juveniles used in the experiments were
artificially hatched and reared at NFI or the Kanagawa Sea
Farming Association. Neogastropods were added to each
container 1 day after the introduction of prey species in all
experiments. When measurements were performed in the
experiments, empty shells of prey species were considered
to be predated individuals, and snails held down by a
predator’s foot were regarded as being captured. In every
experiment, all shells of predated individuals and opercula
of predated T. cornutus were observed to identify the
occurrence and locations of drilled holes.
Observation of predatory behaviors
Preliminary observations of the predatory behaviors of
adults of three species, E. contractus (Muricidae), Eupli-
ca scripta, and Anachis misera (Columbellidae), on
T. cornutus juveniles (7.5 ± 0.9 mm SH; mean ± SD)
310 Fish Sci (2012) 78:309–325
123
Ta
ble
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9
Fish Sci (2012) 78:309–325 311
123
were conducted to examine the manner of attack and
holding exhibited by the three species and the defensive
reactions of T. cornutus juveniles. The predatory gastro-
pods and turban snails were kept for 5 days inside a plastic
basin filled with fully aerated seawater.
In parallel with Experiment 6, the predatory behaviors of
E. contractus on two small gastropods, Cantharidus japo-
nicus and A. misera, were observed in a water tank under
still water conditions. The types of defensive reactions
exhibited by both gastropods were also observed.
Identification of predator
Experiments 1 and 2 were conducted to examine inter-
specific differences in the predation rates of neogastropods
on juvenile turban snails. Adults of three species of
potentially predatory gastropods (E. contractus, E. scripta,
and A. misera) were used in Experiment 1 (Table 2). Eight
turban snail juveniles and three individuals of one of the
three species were placed inside a plastic mesh box
(18.9 9 13.3 9 5.5 cm; mesh size of 1 mm 9 1 mm). In
addition to these three treatments, mesh boxes containing
eight turban snails without predators were prepared as a
control. The boxes were placed on the bottom of a running
seawater tank (65 9 140 9 27 cm).
In Experiment 2, the predation rates on juvenile turban
snails were compared among adult and young individuals
of E. contractus and Thais bronni (Muricidae). Adult
E. contractus, young E. contractus, adult T. bronni, young
T. bronni, and adult E. scripta were used in this experiment
Table 2 Species of neogastropods, shell heights (or shell diameter) of neogastropods and turban snail Turbo cornutus, snails present in each
experimental container, and number of replicates in Experiments 1–5
Neogastropods used as predators Shell height or shell diameter (mm; mean ± SD) Individuals per container Number of replicates
Neogastropods Turban snail Neogastropods Turban snail
Experiment 1
Ergalatax contractus 18.9 ± 1.2 5.7 ± 0.6 3 8 5
Euplica scripta 15.2 ± 1.0 5.7 ± 0.8 3 8 5
Anachis misera 11.3 ± 0.8 5.6 ± 0.9 3 8 5
Experiment 2
Ergalatax contractus 22.8 ± 0.7 7.8 ± 0.6 1 6 6
Young E. contractus 14.0 ± 0.5 7.8 ± 0.6 1 6 6
Thais bronni 27.2 ± 1.3 7.8 ± 0.4 1 6 6
Young T. bronni 17.6 ± 0.4 7.7 ± 0.5 1 6 6
Euplica scripta 14.9 ± 0.5 7.8 ± 0.5 1 6 6
Experiment 3
Juvenile E. contractus 7.7 ± 0.7 1.25 ± 0.12 1 8 6
Enzinopsis menkeana 9.2 ± 0.6 1.27 ± 0.09 1 8 3
Mitrella bicincta 9.8 ± 0.2 1.20 ± 0.14 1 8 4
Juvenile E. scripta 8.3 ± 0.7 1.28 ± 0.10 1 8 4
Anachis misera 6.9 ± 0.6 1.27 ± 0.16 1 8 6
Juvenile T. bronni 7.2 ± 0.8 1.25 ± 0.11 1 8 3
Experiment 4
Ergalatax contractus 21.0 ± 1.3 8.7 ± 0.6 3 8 1
12.2 ± 1.2 3 8 3
17.1 ± 1.1 3 8 3
22.5 ± 1.4 3 5 3
26.9 ± 0.8 3 3 2
Experiment 5
Ergalatax contractus 21.9 ± 1.4 2.8 ± 0.4 1 8 5
1.4 ± 0.2 1 8 5
Young E. contractus 13.9 ± 1.1 2.8 ± 0.4 1 8 5
1.4 ± 0.2 1 8 5
The sizes of the turban snails used in Experiments 3 and 5 are presented above as shell diameters
312 Fish Sci (2012) 78:309–325
123
(Table 2). One individual from each of five groups of
neogastropods and six turban snail juveniles were placed
inside a PVC pipe case (inner diameter of 60 mm and height
of 51 mm) that was enclosed at the top and bottom with
plastic mesh (mesh size of 2 mm 9 2 mm). Ten PVC pipe
cases were placed in a plastic mesh box (34 9 23 9 10 cm;
mesh size of 2 mm 9 7 mm). PVC pipe cases containing
only six turban snail juveniles were prepared as a control
treatment. Four mesh boxes were held 10 cm above the
bottom of the water tank (60 9 90 9 50 cm) on dish
drainer baskets to allow water circulation.
Experiment 3 was conducted to examine the interspecific
differences of predation rates on early juveniles of the tur-
ban snail among neogastropods smaller than those used in
Experiments 1 and 2. In addition to E. contractus, E. scripta,
and T. bronni juveniles, Enzinopsis menkeana (Buccinidae),
Mitrella bicincta (Columbellidae), and A. misera adults
were used as predators in this experiment (Table 2). One
individual of each of the six species and eight early juve-
niles of the turban snail were placed in a 50 ml plastic pot
with 30 ml of filtered seawater (0.45 lm filtered). Pots
containing eight turban snails without neogastropods were
prepared as a control. The plastic pots were maintained at
20�C in an incubator. The filtered seawater in the pots was
exchanged daily. As the number of individuals that could be
collected from the sampling site differed among the neo-
gastropod species, the numbers of replicates for the various
experimental treatments were different (Table 2).
Estimation of prey size
In Experiments 4 and 5, the size range of the turban snail
juveniles that can be predated upon by the muricid gas-
tropod E. contractus was examined. In Experiment 4, the
predation rates of E. contractus on juvenile turban snails of
five size classes were compared to examine the maximum
size of the turban snail upon which this muricid gastropod
can predate (Table 2). The muricid gastropods and the
turban snails of each size class were placed in the same
plastic mesh box as Experiment 1, which were kept at the
bottom of a running seawater tank.
To examine the minimum size of the turban sails that
can be predated upon by E. contractus, the predation rates
of two size classes of E. contractus on early juveniles of
the turban snails of two size classes were compared in
Experiment 5 (Table 2). One E. contractus individual from
each size class and eight turban snails from each size class
were placed inside a plastic bottle connected to a tube
supplying seawater. Many small holes (1 mm in diameter)
were bored on the side of the plastic bottle to allow excess
seawater to overflow. The plastic bottles were placed at the
bottom of the water tank and submerged in discharged
water. For both size classes of turban snail juveniles, five
bottles without E. contractus were prepared as control
treatments.
Examination of the predatory preferences of E. contractus
Three experiments were conducted to examine the preda-
tory preferences of the muricid gastropod E. contractus
among the possible prey species, including T. cornutus.
In Experiment 6, the predation rates of E. contractus on
three small gastropods (juvenile T. cornutus, young Cant-
haridus japonicus, and young A. misera) were compared
under conditions in which each prey species was presented
to E. contractus separately (Table 3). C. japonicus and
A. misera were collected from the field sampling site 2 weeks
before the experiment and maintained in a water tank with
seaweed. To approximately standardize the average SH of the
three prey species, C. japonicus and A. misera were used after
size selection. One individual of E. contractus and eight
individuals of each of the three snail species were introduced
into the same PVC pipe containers used in Experiment 2 and
placed within the same type of mesh box. In addition, three
PVC pipes without E. contractus were prepared for each prey
species as control treatments.
In Experiment 7, the predation rates of E. contractus
(21.0 ± 0.8 mm SH) on juvenile T. cornutus and juvenile
Table 3 Species and shell heights (shell length) of Ergalatax contractus and the prey species, number of E. contractus and turban snails present
in each experimental container, and number of replicates in Experiments 6 and 8
Gastropods used as a prey Shell height or shell length (mm; mean ± SD) Individuals per container Number of
replicatesErgalatax contractus Prey gastropod Ergalatax contractus Prey gastropod
Experiment 6
Turbo cornutus 22.0 ± 1.0 7.8 ± 0.5 1 8 10
Cantharidus japonicus 7.8 ± 0.5 1 8 10
Anachis misera 8.0 ± 0.6 1 8 10
Experiment 8
Haliotis diversicolor 23.4 ± 1.0 8.8 ± 0.8 1 3 10
The sizes of Haliotis diversicolor used in Experiment 8 are presented above as shell lengths
Fish Sci (2012) 78:309–325 313
123
C. japonicus were compared under conditions in which the
two species were presented to the muricid gastropod at the
same time. The juveniles of T. cornutus and C. japonicus
used in this experiment were selected from the same group
used in Experiment 6, and the sizes of the two species
were almost uniform (7.7 ± 0.5 mm, 7.8 ± 0.5 mm SH,
respectively). Three individuals of each of the two species
and one individual of the muricid gastropod were placed
inside a PVC pipe within a mesh box, as in Experiment 6.
When the predated and captured individuals were quanti-
fied, predated juveniles of T. cornutus or C. japonicus were
removed from the container and replaced with living
individuals of almost the same SH.
Experiment 8 was conducted to examine the predation
of E. contractus on the abalone Haliotis diversicolor,
which has a rather differently shaped shell from that of
T. cornutus (Table 3). This abalone species mainly inhabits
boulder areas covered by crustose coralline algae at Nagai,
where E. contractus is also abundant [14]. Juvenile abalone
were artificially hatched and reared at NFI. Three abalone
juveniles were placed inside plastic bottles, as in Experi-
ment 5, and one individual of E. contractus was added.
Four bottles containing abalone juveniles without E. con-
tractus were prepared as a control. The bottles were placed
at the bottom of a water tank and submerged in discharged
water. As the natural water temperature was relatively low
compared to the conditions of the other experiments (April
2009), the discharged water was warmed to maintain the
temperature at 20 �C using a thermostatically controlled
heater.
Data analysis
The predation rates of the neogastropods were calculated at
the end of the experiments. In preliminary observations
performed before Experiments 1 and 6, no individual could
escape from E. contractus once it was held by this preda-
tory gastropod’s foot. Thus, the captured individuals were
considered to be predated in the calculation of the preda-
tion rate of this muricid gastropod:
R ¼ ðpend þ cendÞND
;
where R is the rate of predation by an individual neogas-
tropod (individuals/day), Pend is the number of all predated
individuals throughout the experiments, Cend is the number
of captured individuals at the end of the experiments, N is
the number of neogastropods in each container, and D is
the number of days in the experimental period (eight).
The survival rates of prey species (S) were calculated at
the time when the shells of predated individuals were
quantified in every experiment (except for Experiment 7)
as follows:
St ¼ Lt
ðPtþ Ctþ LtÞ � 100;
where Lt, Pt, and Ct are the number of living, predated, and
captured individuals, respectively, at the time of shell
counting in the experiments.
All statistical analyses were performed using the R 2.6.2
software package [17]. We employed one-way ANOVA
with the Tukey–Kramer HSD test to examine differences in
the predation rates among the experimental treatments in
Experiments 2 and 6, after the data in the experiments had
been confirmed to exhibit homogeneity of variance
(Levene test, p [ 0.05). The differences in the survival
rates of turban snails among the experimental treatments in
Experiment 5 were also examined by one-way ANOVA
with the Tukey–Kramer HSD test. The predation rates of
E. contractus were compared between the two size classes
in Experiment 5 and between the two prey species used in
Experiment 7, and significant differences were tested with
the Mann–Whitney U test.
Results
Field survey
Species composition and density of neogastropods
The density of neogastropods inside ACA turfs at the
sampling site ranged from 160 to 768 individuals/m2 (367
individuals/m2 on average), and neogastropods accounted
for 69.1% of the mollusks collected from the ACA turfs on
average (Fig. 1). The species compositions of the collected
neogastropods according to their densities in terms of
numbers and weights are shown in Figs. 2 and 3, respec-
tively. Among the collected neogastropods, the density of
Euplica scripta was highest, followed by Anachis misera in
terms of numbers. E. scripta was also the most abundant in
terms of weight. A. misera was less abundant in weight
than Pyrene testudinaria tylerae, which was the fourth
highest in terms of numbers. The density of the muricid
gastropod Ergalatax contractus was the third greatest with
respect to numbers and second in terms of weight.
Although the densities of Mitrella bicincta and Enzinopsis
menkeana were not very high among the collected neo-
gastropods, both species appeared throughout the year. The
average number and weight densities of the other species
were less than 10 individuals/m2 and less than 2.0 g/m2 wet
weight.
The composition of the collected E. contractus in terms
of SH is shown in Fig. 4. The sizes of E. contractus ranged
from 4.4 to 23.2 mm SH, and no specific seasonal changes
were found.
314 Fish Sci (2012) 78:309–325
123
Shells of dead turban snails
The size compositions of the dead shells of T. cornutus
collected from the field are shown in Figs. 5 and 6. 88.5%
of the collected turban snail shells were smaller than 2 mm
in shell diameter (Fig. 5), and the number of shells with
diameters of 400–900 lm was greater than in the other size
classes (Fig. 6). A round or elliptical hole (drilled hole)
was found in the dead shells of 28.0% of the turban snails
smaller than 2 mm in shell diameter (125 of 445 shells).
Shell breakage was confirmed in the shells of 10.8% of the
dead turban snails in the \2 mm size class (48 of 445
shells). In addition, a drilled hole was found in 48.3% (28
of 58 shells) of the dead turban snail shells larger than
2 mm in shell diameter, while shell breakage was found in
13.8% (8 of 58 shells). In shells smaller than 2 mm, most
of the drilled holes were at the base of the shell, while
almost all of the drilled holes were found in the upper zone
of the columellar lip among the dead turban snail shells
larger than 2 mm in shell diameter
Den
sity
(in
divi
dual
s/m
2 )
2007 2008 2009 2010 2011
Fig. 1 Abundances of
molluscan species (Gastropoda,
Bivalvia, and Polyplacophora)
collected from assemblages of
articulated coralline algae on
the coast of Nagai, Sagami Bay.
Gastropoda abundance was
divided among three taxonomic
orders (Neogastropoda,
Vetigastropoda, and Discopoda)
and the other orders combined
(Patellogastropoda, Ptenoglossa,
and Aplysiacea)D
ensi
ty (
indi
vidu
als/
m2 )
2007 2008 2009 2010 2011
Fig. 2 Number densities of
gastropod species belonging to
the order Neogastropoda within
assemblages of articulated
coralline algae on the coast of
Nagai, Sagami Bay
Fish Sci (2012) 78:309–325 315
123
Laboratory observations and experiments
Predatory behavior of E. contractus
In preliminary observations performed prior to Experiment
1, only E. contractus was found to predate juveniles of the
turban snail, T. cornutus. Predation by this muricid gas-
tropod on turban snail juveniles was initiated when both
species encountered each other. E. contractus did not
exhibit clear chasing behaviors and did not initiate preda-
tion without a physical contact, even when they came near
a turban snail. At the onset of predatory behavior, an
E. contractus individual contacted the shell or body of a
turban snail with its cephalic tentacles and subsequently
attempted to make contact with its proboscis. When
crawling turban snails encountered E. contractus, they
ceased crawling, retracted their tentacles, and subsequently
withdrew their head–foot into their shell and closed the
aperture using their operculum in almost all cases. How-
ever, this defensive reaction by the turban snail was often
somewhat slower than the rapid action of E. contractus
after making contact. Thus, E. contractus could catch the
Wei
ght d
ensi
ty (
g/m
2 )
Fig. 3 Weight densities of
gastropod species belonging to
the order Neogastropoda within
assemblages of articulated
coralline algae on the coast of
Nagai, Sagami Bay. Others is
the sum of the weight densities
of Strigatella scutula,
Reticunassa multigranasa, and
Ceratostoma fournieri
Freq
uenc
y (%
)
Fig. 4 Size composition of
Ergalatax contractusindividuals collected from turfs
of articulated coralline algae on
the coast of Nagai, Sagami Bay.
The individuals retained in a
3 mm mesh sieve were
measured among the snails
collected in each sampling
316 Fish Sci (2012) 78:309–325
123
head–foot of the turban snail before the closing of the
operculum in some cases. Whether the muricid gastropod’s
attack was faster than the snail’s closing of its operculum
or not, E. contractus continued to hold the turban snail at
the aperture by its sole (Fig. 7). The muricid gastropod
maintained this position for a long period of time, ranging
from several hours to 1 day. As the turban snail’s body was
observed to have disappeared from inside its shell after
E. contractus departed the shell, the turban snail juveniles
appeared to be predated by the gastropod during this
holding period. We did not observe any other predatory
behaviors of this muricid gastropod. E. scripta and A. mis-
era did not show any predatory behavior, even when their
tentacles or proboscis came into contact with the turban
snail juveniles.
The muricid gastropod E. contractus also exhibited
predatory behavior toward C. japonicus and A. misera in the
present study. The predatory behavior of E. contractus
toward these species was almost the same as that toward
T. cornutus, and E. contractus also continued to hold the
apertures of these two prey species. The holding periods
observed for C. japonicus and A. misera were several hours,
and no body tissue was left in the shells held after E. con-
tractus departed. The defensive reactions exhibited by these
two prey species were different from each other, as well as
from that of the turban snail. When a crawling C. japonicus
contacted E. contractus with its cephalic tentacles, the
C. japonicus individual quickly changed its direction of
crawling and visibly increased its crawling speed. When
E. contractus was resting, C. japonicus was often able to
escape from the muricid gastropod. A. misera showed an
offensive reaction, stimulating the approaching head–foot of
E. contractus with its proboscis. The attacked E. contractus
withdrew its tentacles and ceased movement for a short
period, and the predatory behavior was not continued.
0
10
20
30
40
50
60
70
80
90
100
0-1 1-2 2-3 3-4 4-5 5-6 6-7 7-8 8-9 9-10 10-
0
50
100
150
200
250
300
350
400
with shell breakage
with drilled hole
without drilled hole or shell breakage
Freq
uenc
y (%
)
Shell height or shell diameter (mm)
Num
ber
of d
ead
turb
an s
nail
s
Fig. 5 Size composition of shells of dead Turbo cornutus collected
from the coast of Nagai, Sagami Bay (above) and the percentages of
shells with a drilled hole or shell breakage in each size class (below).
The sizes of early juvenile turban snails less than 3.5 mm in shell
height correspond to shell diameters
with shell breakage
with drilled hole
without drilled hole or shell breakage
Num
ber
of d
ead
turb
an s
nail
sFr
eque
ncy
(%)
Shell diameter (µm)
Fig. 6 Size composition of shells of dead Turbo cornutus collected
from the coast of Nagai, Sagami Bay, among individuals smaller than
2 mm in shell diameter (above), and the percentages of dead shells
with a drilled hole or shell breakage in each size class (below)
Fig. 7 Ergalatax contractus (gray arrow) predating a juvenile of
Turbo cornutus (white arrow)
Fish Sci (2012) 78:309–325 317
123
Identification of predators
No dead individuals of the four prey species were found in
the control treatments for any of the experiments, with the
exception of Experiment 5 (see below), and no visible
abnormalities were detected in the living prey snails. Thus,
the death of the prey species was not thought to be caused
by starvation or disease, but by predation by the neogas-
tropods. In addition, no snail used as a predator died in any
of the experiments.
The numbers of living, captured, and predated turban
snails and the predation rates of the neogastropods in
Experiments 1–3 are shown in Table 4. In Experiment 1,
only E. contractus predated upon the turban snail juveniles,
and the average survival rates of the turban snail juveniles
after 4 and 8 days were 42.5 and 2.5%, respectively. No
dead turban snail was found in the treatments in which E.
scripta or A. misera was employed as a predator. All 39
individuals of T. cornutus predated by E. contractus
exhibited a drilled hole in the upper zone of the columellar
lip (Table 5; Fig. 8a).
The turban snail juveniles were predated by the two spe-
cies of Muricidae in Experiment 2. The predation rate of
adult E. contractus (0.40 ± 0.09 individuals/day) was sig-
nificantly higher than those of the other predators, except for
young E. contractus (ANOVA with Tukey–Kramer
HSD test, p \ 0.01). The predation rate of young E. con-
tractus (0.29 ± 0.09 individuals/day) was significantly
higher than those of adult and young T. bronni (ANOVA
with Tukey–Kramer HSD test, p \ 0.01). No significant
differences were found among the predation rates of
E. scripta and adult and young T. bronni (ANOVA with
Tukey–Kramer HSD test, p [ 0.05) (0.00 ± 0.00 individ-
uals/day, 0.06 ± 0.06 individuals/day, and 0.08 ± 0.06
individuals/day, respectively). In almost all shells of turban
snails predated by adult E. contractus, a drilled hole was left
in the upper zone of the columellar lip (Table 5). Although
there was no visible hole or breakage in the shells of dead
individuals predated by adult and young T. bronni
(Table 5), semicircular breakages were found on the margin
of the operculum in two individuals predated by young
T. bronni (Fig. 9).
In Experiment 3, only juveniles of E. contractus pre-
dated the early juveniles of the turban snail, and the pre-
dation rate by this muricis gastropod was 1.13 ± 0.59
individuals/day (Table 4). All 27 individuals of T. cornutus
predated by juvenile E. contractus exhibited a drilled hole
in the base of the body whorl (Table 5; Fig. 8b).
Estimation of prey size
In Experiment 4, using turban snail juveniles of five dif-
ferent size classes, juveniles belonging to the 5–10 mm SH
and 10–15 mm SH size classes were found to be predated
by the muricid gastropod, whereas no turban snails in the
other size classes were predated during the experimental
period. The predation rates of E. contractus on turban snail
juveniles in the 5–10 mm SH and 10–15 mm size classes
were 0.25 individuals/day and 0.15 ± 0.02 individuals/
day, respectively. The turban snail juveniles were re-cate-
gorized into nine size classes with 2.5 mm SH intervals,
and the numbers of living and predated individuals in each
size class at the end of the experiment are shown in Fig. 10.
The maximum size among the predated juveniles was
13.8 mm SH, and individuals larger than 15 mm SH were
not predated by E. contractus. The percentage of individ-
uals drilled by E. contractus was greater in the 5–10 mm
SH size class than in the 10–15 mm SH size class, and only
one individual among 11 turban snails was drilled in the
treatment using juveniles of the 10–15 mm SH size class
(Table 5).
In Experiment 5, using early juvenile turban snails of
two different size classes, dead early juveniles were found
in all of the experimental treatments, including the control
treatment. Among the three treatments employing early
juveniles with a 2.8 mm shell diameter, the survival rate of
early juveniles in the treatment with young E. contractus
was significantly lower than that in the treatment using
adult E. contractus and the control treatment (ANOVA
with Tukey–Kramer HSD test, p \ 0.05) (Fig. 11). The
predation rate of young E. contractus on turban snails of
this size (0.83 ± 0.19 individuals/day) was significantly
higher than that of adult E. contractus (0.28 ± 0.18 indi-
viduals/day) (Mann–Whitney U test, p \ 0.05). Among the
three treatments using early juveniles with a shell diameter
of 1.4 mm, the survival rate in the treatment using young
E. contractus was significantly lower than that in the
treatment using adult E. contractus on every measurement
day, but it was not significantly different from that in the
control treatment at the end of the experiment (Fig. 12).
The predation rate of young E. contractus on turban snail
early juveniles of this size (0.33 ± 0.12 individuals/day)
was significantly higher than that of adult E. contractus
(0.03 ± 0.05 individuals/day) (Mann–Whitney U test,
p \ 0.05). In this experiment, shell breakages that were
larger than drilled holes were found on some dead shells.
The shells of seven early juveniles with a shell diameter of
2.8 mm predated by young E. contractus were heavily
damaged around the columellar lip. The shells of two dead
individuals with a shell diameter of 1.4 mm in the treat-
ment using adult E. contractus exhibited extensive break-
age, and almost the entire base of the shell disappeared.
With respect to early juveniles with a shell diameter of
1.4 mm that were predated by young E. contractus, three
shells lost most of the whorl or base, and another three
shells were heavily damaged around the aperture.
318 Fish Sci (2012) 78:309–325
123
Ta
ble
4N
um
ber
so
fli
vin
g,
cap
ture
d,
and
pre
dat
edju
ven
iles
of
Tu
rbo
corn
utu
sin
each
exp
erim
enta
ltr
eatm
ent
inE
xp
erim
ents
1–
3,
and
pre
dat
ion
rate
so
fm
uri
cid
snai
lsu
sed
asp
red
ato
rs
Sn
ails
use
das
pre
dat
ors
Ind
ivid
ual
s(m
ean
±S
D)
Pre
dat
ion
rate
(in
div
idu
als/
day
)
(mea
n±
SD
)2
day
s4
day
s6
day
s8
day
s
Liv
ing
Cap
ture
dP
red
ated
Liv
ing
Cap
ture
dP
red
ated
Liv
ing
Cap
ture
dP
red
ated
Liv
ing
Cap
ture
dP
red
ated
Ex
per
imen
t1
Erg
ala
tax
con
tra
ctu
s–
––
3.4
±1
.41
.2±
0.7
3.4
±1
.2–
––
0.2
±0
.40
7.8
±0
.40
.33
±0
.00
Eu
pli
casc
rip
ta–
––
8.0
±0
.00
0–
––
8.0
±0
.00
00
An
ach
ism
iser
a–
––
8.0
±0
.00
0–
––
8.0
±0
.00
00
Ex
per
imen
t2
Erg
ala
tax
con
tra
ctu
s5
.5±
0.5
00
.5±
0.5
4.7
±0
.50
1.3
±0
.54
.2±
0.4
01
.8±
0.4
2.8
±0
.70
.5±
0.5
2.7
±0
.50
.40
±0
.09
Yo
un
gE
.co
ntr
act
us
5.0
±0
.60
1.0
±0
.64
.8±
0.4
01
.2±
0.4
4.5
±0
.50
1.5
±0
.53
.7±
0.7
02
.3±
0.7
0.2
9±
0.0
9
Th
ais
bro
nn
i6
.0±
0.0
00
5.8
±0
.40
0.2
±0
.45
.8±
0.4
00
.2±
0.4
5.5
±0
.50
0.5
±0
.50
.06
±0
.06
Yo
un
gT
.b
ron
ni
5.8
±0
.40
0.2
±0
.45
.7±
0.5
00
.3±
0.5
5.5
±0
.50
0.5
±0
.55
.3±
0.5
00
.7±
0.5
0.0
8±
0.0
6
Eu
pli
casc
rip
ta6
.0±
0.0
00
6.0
±0
.00
06
.0±
0.0
00
6.0
±0
.00
00
Ex
per
imen
t3
Juv
enil
eE
.co
ntr
act
us
5.5
±2
.20
2.5
±2
.23
.5±
2.4
04
.5±
2.4
––
––
––
1.1
3±
0.5
9
En
zin
op
sis
men
kea
na
8.0
±0
.00
08
.0±
0.0
00
8.0
±0
.00
08
.0±
0.0
00
0
Mit
rela
bic
inct
a8
.0±
0.0
00
8.0
±0
.00
08
.0±
0.0
00
8.0
±0
.00
00
Juv
enil
eE
.sc
rip
ta8
.0±
0.0
00
8.0
±0
.00
08
.0±
0.0
00
8.0
±0
.00
00
An
ach
ism
iser
a8
.0±
0.0
00
8.0
±0
.00
08
.0±
0.0
00
8.0
±0
.00
00
Juv
enil
eT
.b
ron
ni
8.0
±0
.00
08
.0±
0.0
00
8.0
±0
.00
08
.0±
0.0
00
0
Fish Sci (2012) 78:309–325 319
123
Fig. 8 Shells of dead Turbo cornutus juveniles predated by
Ergalatax contractus in Experiment 2 (a) and Experiment 3 (b). In
the shells from Experiment 2, a drilled hole made by E. contractus
was observed in the upper zone of the columellar lip. In the dead
shells of T. cornutus juveniles from Experiment 3, a drilled hole made
by E. contractus was left on the base of the shell
Table 5 Numbers of dead shells of Turbo cornutus with a drilled hole, with extensive breakage, and with no drill hole and no breakage in
laboratory experiments
Neogastropods
used as predators
Average size of
juvenile turban snails
With a drilled hole With
extensive
breakage
With no drilled hole
and no shell breakage
Percentage with
a drilled shellOn the upper zone
of the columellar lip
On the body
whorl
Experiment 1
Ergalatax contractus 5.7 mm in shell height 39 0 0 0 100.0
Experiment 2
E. contractus 7.8 mm in shell height 14 1 0 1 93.8
Young E. contractus 7 1 0 6 57.1
Thais bronni 0 0 0 3 0.0
Young T. bronni 0 0 0 4 0.0
Experiment 3
Juvenile E. cornutus 1.3 mm in shell diameter 0 27 0 0 100.0
Experiment 4
E. contractus 8.7 mm in shell height 6 0 0 0 100.0
12.2 mm in shell height 1 0 0 10 9.1
Experiment 5
E. contractus 2.8 mm in shell diameter 9 2 0 0 100.0
Young E. contractus 15 7 7 4 66.7
E. contractus 1.4 mm in shell diameter 0 0 2 0 0.0
Young E. contractus 4 3 6 0 53.8
Experiment 6
E. contractus 7.8 mm in shell height 24 0 0 8 75.0
Experiment 7
E. contractus 7.7 mm in shell height 14 1 0 10 60.0
320 Fish Sci (2012) 78:309–325
123
The numbers of living, captured and predated prey spe-
cies and the predation rates of E. contractus on each prey
species in Experiment 6 are shown in Table 6. E. contractus
predated on the T. cornutus juveniles most actively, and
their predation rate on the turban snail (0.40 ± 0.10 indi-
viduals/day) was significantly higher than those on
C. japonicus and A. misera (ANOVA with Tukey–Kramer
HSD test, p \ 0.05) (0.16 ± 0.10 and 0.09 ± 0.08 indi-
viduals/day, respectively). A drilled hole was found on the
upper zone of the columellar lip in 24 individuals among the
32 turban snail juveniles predated in this experiment
(Table 5). No visible drilled hole or breakage was observed
in the shells of predated C. japonicus and A. misera.
In Experiment 7, where E. contractus could choose to
prey upon T. cornutus and C. japonicus, the predation rate
on C. japonicus was 0.01 ± 0.04 individuals/day. This
predation rate was much lower than that found in Experi-
ment 6. The predation rate on the turban snail juveniles was
0.39 ± 0.12 individuals/day, which was equivalent to that
in Experiment 6 and significantly higher than the predation
rate on C. japonicus in this experiment (Mann–Whitney U
test, p \ 0.01). The occurrence and positions of the drilled
holes in the dead shells of the turban snail in this experi-
ment are presented in Table 5. As in Experiment 6, no
visible breakage was found in the predated C. japonicus.
Fig. 9 Shell (a) and operculum (b) of a dead Turbo cornutus juvenile that was predated by Thais bronni in Experiment 2. Semicircular breakage
occurred at the margin of the operculum (inside broken line)
Shell height (mm)
Num
ber
of in
divi
dual
s
0
4
8
12
16
7.5-
10.0
10.0
-12.
5
12.5
-15.
0
15.0
-17.
5
17.5
-20.
0
20.0
-22.
5
22.5
-25.
0
25.0
-27.
5
27.5
-30.
0
survived
predated
Fig. 10 Size compositions of the surviving and predated juveniles of
Turbo cornutus in Experiment 4
Surv
ival
rat
e (%
)
Days
A
A
B
a
a
b
1
1
2
0
25
50
75
100
0 2 4 6 8
With adult predatory snail
With young predatory snail
Control
Fig. 11 Survival rates of early juvenile Turbo cornutus (2.8 mm in
shell diameter on average) in the three experimental treatments of
Experiment 5. Vertical bars indicate the standard deviation. Meanvalues marked with different letters or numbers indicate that there is a
significant difference between these values (ANOVA with Tukey–
Kramer HSD test, p \ 0.05)
Fish Sci (2012) 78:309–325 321
123
The predation rate of E. contractus on the abalone
H. diversicolor was very low (0.03 ± 0.05 individuals/
day), and the survival rate of the abalone at the end of the
experiment (93.3 ± 13.3%) was not significantly different
from that in the control experiment (100 ± 0.0%) (Mann–
Whitney U test, p [ 0.05). When abalone juveniles
encountered E. contractus, they changed their crawling
direction and increased their crawling speed to escape from
E. contractus. Even when the muricid gastropod’s foot was
on the shell of the abalone, the abalone could escape. The
shells of the two dead abalones did not exhibit any drilled
hole or breakage.
Discussion
Predatory behavior of neogastropods
The muricid gastropod E. contractus showed apparent
behaviors of an active predator toward T. cornutus and the
other gastropods, although E. contractus has been thought to
be a scavenger or opportunistic predator [12, 18]. This is the
first report on the active predation of E. contractus on these
gastropods based on experimental evidence. The predation
rates of this species on juveniles and early juveniles of the
turban snail were significantly higher than those of the other
investigated neogastropods in all of the experiments. As
E. contractus is one of the dominant species inside the ACA
turfs throughout the year, this muricid gastropod is likely to
be an influential predator in the macroinvertebrate assem-
blages associated with the ACA turfs. Thais bronni also
exhibited predatory behavior toward the turban snail juve-
niles, but the predation rate of T. bronni was lower than that
of E. contractus. The abundance of T. bronni was much
lower inside the ACA turfs, and its ability to capture moving
Surv
ival
rate
(%
)
Days
2
a
ab
b
A
AB
B
1 1
0
25
50
75
100
0 2 4 6 8
With adult predatory snail
With young predatory snail
Control
Fig. 12 Survival rates of early juveniles Turbo cornutus (shell
diameter of 1.4 mm on average) in the three experimental treatments
of Experiment 5. Vertical bars indicate the standard deviation. Meanvalues marked with different letters or numbers indicate that there is a
significant difference between these values (ANOVA with Tukey–
Kramer HSD test, p \ 0.05)
Ta
ble
6N
um
ber
so
fli
vin
g,
cap
ture
d,
and
pre
dat
edin
div
idu
als
of
thre
ep
rey
spec
ies
inE
xp
erim
ent
6,
and
pre
dat
ion
rate
so
fE
rga
lata
xco
ntr
act
us
on
each
pre
ysp
ecie
s
Gas
tro
po
ds
use
d
asp
rey
Ind
ivid
ual
s(m
ean
±S
D)
Pre
dat
ion
rate
(in
div
idu
als/
day
)
(mea
n±
SD
)2
day
s4
day
s6
day
s8
day
s
Liv
ing
Cap
ture
dP
red
ated
Liv
ing
Cap
ture
dP
red
ated
Liv
ing
Cap
ture
dP
red
ated
Liv
ing
Cap
ture
dP
red
ated
Tu
rbo
corn
utu
s5
.4±
0.5
0.2
±0
.40
.4±
0.5
4.5
±0
.80
.2±
0.4
1.3
±0
.83
.9±
0.7
02
.1±
0.7
2.8
±0
.70
.4±
0.5
2.8
±0
.70
.40
±0
.10
Ca
nth
ari
du
sja
po
nic
us
5.7
±0
.50
0.3
±0
.55
.3±
0.6
00
.7±
0.6
4.9
±0
.80
1.1
±0
.84
.7±
0.8
01
.3±
0.8
0.1
6±
0.1
0
An
ach
ism
iser
a5
.7±
0.5
0.1
±0
.30
.2±
0.4
5.6
±0
.50
0.4
±0
.55
.5±
0.5
00
.5±
0.5
5.3
±0
.60
0.7
±0
.60
.09
±0
.08
322 Fish Sci (2012) 78:309–325
123
snails was apparently poorer than that of E. contractus. Thus,
the predatory influence of T. bronni on small gastropods may
be less than that of E. contractus within ACA turfs. As
T. bronni has been observed to actively predate the blue
mussel Mytilus galloprovincialis and the Japanese cockle
Venerupis philippinarum under the rearing conditions at
AMBS (Hayakawa, personal observation), T. bronni may
prefer bivalves within ACA turfs, such as Hiatella orientalis
and Cardita leana. Although columbellid species have
generally been considered to be predatory snails, some of
these species have been reported to be herbivorous gastro-
pods [19]. The two investigated species of the family Col-
umbellidae, Euplica scripta and Anachis misera, did not
exhibit predatory behavior toward juveniles of T. cornutus.
The two species did not even hold the turban snail juveniles,
and the juveniles did not show any apparent defensive
reactions. Thus, it is concluded that Euplica scripta and
Anachis misera are not predators for T. cornutus during early
life stages. As these two species were found to be dominant
inside the ACA turfs, their feeding habitat should be iden-
tified by further research in order to clarify the food web
structure inside ACA turfs.
Prey size of E. contractus
In the experiments described herein, adult E. contractus
approximately 20 mm in SH actively predated turban snail
juveniles in the size range 5–13 mm in SH, while the
muricid gastropod exhibited almost no predation of early
juveniles less than 3 mm in shell diameter. However,
young E. contractus approximately 13 mm in SH and
juvenile E. contractus approximately 8 mm in SH were
found to predate early juveniles with shell diameters of less
than 3 mm. Based on this result, the size range of turban
snails that can be predated by E. contractus appears to be
related to the SH of this muricid species—similar to pre-
viously reported relationships between the size of preda-
tory muricid gastropods and prey species [20, 21]. The
turban snail T. cornutus inhabits ACA turfs for approxi-
mately 1 year following settlement, and juveniles that grow
to approximately 15 mm SH are thought to depart the ACA
turfs [22]. The results of the present study indicate that
E. contractus individuals of a wide size range inhabit ACA
turfs at relatively high densities at Nagai in Sagami Bay.
Thus, turban snails seem to experience continuous high
predation pressure from E. contractus throughout their
early life stages when they use ACA turfs as a nursery.
Defensive reaction of prey species against predation
by E. contractus
Although the calcified operculum characteristic of the
family Turbinidae is thought to be a passive armor against
predation [23], it has been reported that the turban snail
Lunella coronata is predated by the muricid gastropod
Reishia clavigera, which is able to drill a hole into the
snail’s shell [24]. In the present study, it was also observed
that T. cornutus were easily predated via the drilling of the
muricid species E. contractus. Therefore, the calcified
operculum of the turban snails was not found to be an
effective defensive organ for protection against a drilling
attack from these predatory gastropods. In contrast, the
predation rates on C. japonicus, A. misera, and H. diver-
sicolor by E. contractus were all lower than that for the
turban snail. Thus, defensive reactions such as immediate
flight after contact with E. contractus (C. japonicus and
H. diversicolor) and counterattack using the proboscis
(A. misera) were considered to be imperfect but effective
defensive reactions against predation by E. contractus. The
prey preferences of predatory gastropods are considered to
be affected by various characteristics of prey species, such
as their defensive reactions, shell morphology, and size
[25–27]. The muricid gastropod E. contractus appeared to
preferentially predate T. cornutus rather than C. japonicus
based on the results of the present laboratory experiment,
and this preference may be affected by the effectiveness of
the defensive reactions of the prey species.
Drilled holes as evidence of neogastropod predation
High percentages (60–100%) of the shells of the turban snail
juveniles 5–9 mm in SH that were predated by adult
E. contractus in this study were drilled (Table 5). The drilled
holes were predominantly located in the upper zone of the
columellar lip. This localization of the penetration point was
considered to be derived from the muricid gastropod’s pos-
ture of attack, covering the turban snail’s aperture. In this
posture, the head of E. contractus is located around the upper
zone of the columellar lip. Although the holes drilled by
E. contractus were left on the base of the shell in Experiment
3, this is because the aperture of the early juveniles was
small, and the head of E. contractus was situated at the base
of the shell. In some predated individuals, a drilled hole was
observed in the upper zone of the whorl; however, the attack
posture of the snails that made such a drilled hole was not
observed in this study. When several E. contractus individ-
uals were observed attacking one turban snail juvenile in the
field, one E. contractus individual was found to hold the
aperture while the others attached to the upper zone of the
whorl (Hayakawa, personal observation). As a drilled hole
on the whorl was even found in the experiments using one
predator per container, E. contractus is probably able to
penetrate not only the upper zone of the columellar lip but
also a wide area of the shell of a turban snail juvenile. In
contrast, no drilled holes were found on the shells of the
turban snail juveniles predated by T. bronni. Some muricid
Fish Sci (2012) 78:309–325 323
123
gastropods, such as Dicathais orbita and Neorapana tuber-
culata, have been reported to drill the marginal areas of the
opercula of turbinid gastropods [28, 29], and small missing
fragments were confirmed in the marginal areas of some
individuals predated by T. bronni in this study. Thus, the
style of predation on the turban snail gastropods was con-
sidered to differ among the species of predatory gastropods.
The occurrence and position of the hole drilled by
E. contractus varied depending on the sizes of this muricid
snail and the predated turban snail. In the shells of predated
turban snail juveniles larger than 10 mm in SH, no drilled
holes or breakages were found, except in one individual in
Experiment 4. As the thickness of the snail’s shell increases
with growth, even adult E. contractus seem to be unable to
penetrate the shells of turban snail juveniles larger than
10 mm in SH. This muricid snail may predate turban snails
of those sizes only when they succeed in holding the head–
foot before the turban snail closes its aperture with its
operculum. In contrast, areas of breakage larger than the
drilled holes were found on the shells of turban snail
juveniles with shell diameters of less than 3 mm that were
predated by adult and young E. contractus. This may be
because the shell of the turban snail early juvenile is too
small for the radula of the adult E. contractus, and so thin
that drilling readily damages a wider area than the limited
drilled point. In Experiment 3 using early juveniles of the
turban snail with a shell diameter of 1.25 mm, a complete
drilled hole was left in every shell predated by juvenile
E. contractus. Thus, small juveniles of E. contractus could
drill through the shells of early juvenile turban snails
without causing extensive breakage of the shell. As the
predation rate on smaller turban snails was higher among
smaller E. contractus, a cost–benefit relationship was
assumed to exist between the sizes of the turban snails and
the muricid gastropod.
E. contractus as a predator for juvenile T. cornutus
Drilled holes were also observed in the dead shells of turban
snail juveniles collected from the field. The percentages of
shells with a drilled hole tended to increase among larger
juveniles, especially among early juveniles smaller than
2 mm in shell diameter (Figs. 5, 6). The shape and position of
the drilled holes in the shells collected from the field were
similar to those found aming the predated turban snails in the
laboratory experiments (Fig. 13). Among the dominant spe-
cies of neogastropods within ACA turfs, only E. contractus
was found to leave drilled holes on predated individuals, so
the dead shells of turban snail juveniles collected from the
field were considered to have been predated by E. contractus.
E. contractus juveniles smaller than 7 mm SH are assumed to
be influential predators for early juveniles of the turban snail,
because the drilled holes in the collected dead shells were
smaller than the drilled holes made by the juvenile E. con-
tractus in Experiment 3, and the size of the hole drilled by a
muricid species is reported to be proportional to the size of
the muricid species [21, 30]. Considering the high percentage
of ddead shells of turban snail juveniles that were found to
exhibit drilled holes, predation by E. contractus seems to be a
key factor in the mortality of T. cornutus in its early life
stages. Regardless of the precise rates of predation by this
muricid gastropod, predation by this species may have a
strong impact on the population dynamics of small gastro-
pods, especially species that do not exhibit an effective
defense strategy against drilling on their shells.
As predation by E. contractus appeared to be triggered by
incidental encounters, the complex physical structure of
ACA turfs may moderate the negative impact of this muricid
gastropod’s predation on the T. cornutus juveniles inhabit-
ing these turfs. Previous studies have indicated that ACA
turfs represent important settlement substrata for larvae of
Fig. 13 Dead shells from a Turbo cornutus juvenile (a) and early juveniles (b) collected from the field sampling site, all with drilled holes.
Drilled holes are located at the heads of the gray arrows in the upper zone of the columellar lip (a) and on the base of the shell (b)
324 Fish Sci (2012) 78:309–325
123
turban snails [8, 31] and provide suitable diets for juvenile
turban snails [32]. To understand the ecological importance
of ACA turfs as nurseries for gastropods, including Japanese
spiny turban snail T. cornutus, further research will be
needed to reveal the function of these turfs as protective
shelters against predation by predatory gastropods as well as
other possible predators, such as crabs and wrasses.
Acknowledgments The authors thank the staff of the Nagasaki Pre-
fectural Institute of Fisheries for their cooperation in rearing larvae and
juveniles of turban snails. We are also grateful to the staff of the National
Research Institute of Fisheries Science for their kind help in carrying out
the experiments. This research was partly supported by a Grant-in-Aid
for Scientific Research from the Japan Society for the Promotion of
Science (JSPS) to T. Kawamura (no. 20380108). J. Hayakawa was also
financially supported by a research fellowship from JSPS.
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