Journal of
The Malacological Society of London
Molluscan Studies
Journal of Molluscan Studies (2012) 78: 205–212. doi:10.1093/mollus/eys002
SIZE-SELECTIVE PREDATION AND DRILLHOLE-SITE
SELECTIVITY IN EUSPIRA FORTUNEI (GASTROPODA:
NATICIDAE): IMPLICATIONS FOR ECOLOGICAL
AND PALAEOECOLOGICAL STUDIES
TOMOKI CHIBA 1 AND SHIN’ICHI SATO 2
1
Institute of Geology and Paleontology, Graduate School of Science, Tohoku University, Aoba 6-3, Aramaki, Aoba-ku, Sendai 980-8578, Japan;
and 2The Tohoku University Museum, Aoba 6-3, Aramaki, Aoba-ku, Sendai 980-8578, Japan
Correspondence: T. Chiba; e-mail: [email protected]
(Received 20 October 2011; accepted 23 December 2011)
ABSTRACT
We explored the prey-size preference and drillhole-site selectivity in Euspira fortunei preying on
Ruditapes philippinarum by means of laboratory experiments. Euspira fortunei was a size-selective predator and there was a positive correlation between predator and prey sizes. Our experiments and observations showed that prey-size limits in E. fortunei were determined by the size of its foot, which is the
organ used for capturing and handling prey, as in other naticid species. Within the manipulation
limits, attacks on relatively small or large prey were detected after prey of the preferred size classes
became scarce. Our experiments also suggested that there was no size refuge for R. philippinarum (shell
length range 0– 35 mm) from attack by E. fortunei and that R. philippinarum of shell length range 10 –
25 mm were especially vulnerable to predation. These results imply that introduction of E. fortunei
probably causes significant loss in R. philippinarum stocks. The sizes of E. fortunei individuals were significantly correlated with the diameters of the drillholes left on the shells of prey. Drillhole location
was generally stereotypical in size-matched prey but anomalous drillhole placements commonly occurred in size-mismatched prey. Because E. fortunei captured prey using its foot and manipulated prey
in a stereotypical manner, handling of size-mismatched prey was difficult and thus attacks on such
prey tended to result in anomalous drillhole placements. Euspira fortunei did not make drillholes on
the edges of bivalve prey when it competed for prey.
INTRODUCTION
Marine invertebrate shell-drilling predators are of interest to
both ecologists and palaeoecologists. Significant among such
predators are the naticids and muricids, which feed on shelled
prey. In many aquatic communities, both naticids (Franz,
1977; Wiltse, 1980a; Commito, 1982; Beal, 2006; Quijón,
Grassle & Rosario, 2007) and muricids (Connell, 1970; Katz,
1985; Navarrete & Menge, 1996) play an important role in
regulating the community structure and size-frequency distribution of their prey. In addition, predatory drillholes represent
an important source of information about the nature of past
biotic interactions that can be studied and analysed quantitatively (e.g. Kitchell, 1986; Kowalewski, 2002; Leighton, 2002).
Furthermore, both prey and predator have high preservation
potential and a rich fossil record because of their calcareous
exoskeletons.
Laboratory experiments help ecologists understand the potential impact of shell-drilling predators on prey populations
and community structure, by revealing the consumption rate
and prey preferences of a predator (e.g. Peharda & Morton,
2006; Savini & Occhipinti-Ambrogi, 2006). For palaeoecologists, laboratory experiments provide an important biological
context and can be used to interpret information, such as
predator size (Kitchell et al., 1981), predator identity (Dietl &
Kelley, 2006), prey-size selectivity (Kitchell, 1986) and the intensity of competition for prey (Dietl, Herbert & Vermeij,
2004), that can be extracted from the fossil record of drillholes.
The naticid gastropod Euspira fortunei (Reeve, 1855) was unintentionally introduced to northern Japan from China or
Korea with imported seed of the commercial clam Ruditapes
philippinarum (Adams & Reeve, 1850). Okoshi (2004) showed
that E. fortunei was mixed in the sacks filled with R. philippinarum imported from China to Miyagi Prefecture, northern
Japan in 2002. After the invasion of E. fortunei, populations of
R. philippinarum, which is the preferred prey for E. fortunei,
decreased dramatically in recipient communities (Sakai, 2000;
Okoshi & Sato-Okoshi, 2011).
# The Author 2012. Published by Oxford University Press on behalf of The Malacological Society of London, all rights reserved
T. CHIBA AND S. SATO
The first aim of this study is to describe the size-selective predation by E. fortunei. Size-selective predation is a potentially
important factor that affects the size-frequency distribution of
prey, because it may lead to the depletion of certain prey-size
classes (Kitching, Sloane & Ebling, 1959; Ebling et al., 1964;
Paine, 1974, 1976; Franz, 1977; Commito, 1982; Summerson &
Peterson, 1984). The second aim is to elucidate the mechanics
of selecting drillhole locations and the cause of anomalous
drillhole placements by E. fortunei. Hasegawa & Sato (2009)
stated that drillholes produced by E. fortunei were countersunk
and commonly located around the umbo of R. philippinarum
valves. In our personal observation, however, E. fortunei sometimes leaves drillholes in the centre of R. philippinarum valves. It
is generally believed that the consistent (stereotypical) placement of naticid drillholes on the shells of prey is the consequence of a fixed behavioural pattern of manipulating and
orientating the prey (Kitchell et al., 1981). As predicted by
Kitchell et al. (1981), stereotypical distributions of naticid drillholes have been widely reported (e.g. Taylor, 1970; Berg &
Nishenko, 1975; Griffiths, 1981; Kelley, 1988; Dietl &
Alexander, 1997); however, anomalous drillhole distributions
have also been reported (e.g. Kabat & Kohn, 1986; Anderson,
1992). Dietl et al. (2004) showed that the muricid gastropod
Chicoreus dilectus usually drilled the shell wall of Chione elevata,
but the predator tended to drill the shell edge when it competed for prey. Such alternative shell-drilling behaviours may
explain anomalous drillhole placements of naticids, although
no previous study has tested this hypothesis. In this study, we
examine whether E. fortunei likewise shifts drillhole locations
when it competes for prey.
Figure 1. Map showing the sampling localities. A. Japan with the
location of the coastal area of Miyagi Prefecture highlighted. B.
Enlarged coastal area of Miyagi Prefecture highlighting location of the
Tona coast and the Gamo tidal flat. Individuals of Euspira fortunei and
Ruditapes philippinarum were collected from Tona and Gamo,
respectively.
MATERIAL AND METHODS
Source of predators and prey
In April and June 2010, about 130 individuals of Euspira fortunei
were opportunistically collected by hand from the tidal flat at
Tona, Higashi-Matsushima City, Miyagi prefecture, northern
Japan (388210 N 141080 E; Fig. 1). Between April 2010 and
January 2011, about 600 individuals of Ruditapes philippinarum
were collected by hand from the tidal flat at Gamo, Sendai City,
Miyagi prefecture, northern Japan (388250 N 1418010 E; Fig. 1).
The animals were brought back to the laboratory and maintained in plastic tanks that were placed together in two large
glass tanks (tank 1: 30 60 cm, 40 cm high; tank 2: 40 50 cm, 70 cm high) with filtered running seawater. The plastic
tanks were partially filled with a 5–10-cm thick layer of
coarse sand or clear beads. We confirmed that E. fortunei and
R. philippinarum could burrow into both substrata. During the
experiments, the temperature of the seawater remained at
15.0 –22.08C, which is similar to monthly mean sea-surface
temperature between May and June 2010 at c. 3 km south
of Tona (May: 15.58C, June: 21.28C; Hydrographic and
Oceanographic Department 2nd Regional Coast Guard
Headquarters, 2011).
various sizes were offered in each tank: four prey clams from
each of the seven size classes were introduced into each of the
11 plastic tanks. We avoided providing more clams because
this may restrict predatory behaviour of E. fortunei. We sifted
out animals from substrata at least twice per week. Some clams
seemed to die as a result of starvation or stress rather than
naticid predation, because there was soft tissue in the dead
shells. Such dead clams were replaced with another clam of the
same size class. When an E. fortunei individual killed a clam
and abandoned it, the dead shell was removed from the tank
and it was not replaced. The experiments were conducted over
two periods: 6 October 2010 to 4 January 2011, and 21
November 2010 to 19 February 2011 (Table 1). We recorded
the number of clams that were consumed and the date when
each clam was consumed. The lengths of the drilled shells were
measured to the nearest 0.01 mm using a digital calliper. Prey/
predator size ratios (prey size divided by predator size) were
calculated. In these calculations, the predator sizes in tanks
A –K were approximated as 12, 14, 16, 18, 20, 22, 24, 26, 28,
30 and 32 mm, respectively. The drillhole locations on both
the right and left valves were categorized using the zones
shown in Figure 3.
Prey-size preference and drillhole-site selectivity
Relationships between predator size and drillhole diameter
Euspira fortunei individuals were divided into 11 size classes
(shell height: 11– 13, 13–15, 15–17, 17–19, 19–21, 21–23,
23– 25, 25–27, 27 –29, 29– 31 and 31–33 mm; Fig. 2).
Predators were individually placed into separate plastic tanks
(tanks A– K; Table 1). The prey, R. philippinarum, were divided
into seven size classes (shell length: 0– 5, 5–10, 10–15, 15– 20,
20– 25, 25–30 and 30 –35 mm; Fig. 2). Twenty-eight clams of
To examine the relationships between predator size and drillhole diameter, the following experiments were conducted
between 6 June and 8 November 2010. Euspira fortunei individuals between 6.05 and 38.55 mm in shell height were individually placed into separate plastic tanks (5.7 8.2 cm,
10.5 cm high) with several prey clams. If the predators consumed the clams, the size of the predator (shell height) and
Experimental design
206
STEREOTYPICAL PREDATION IN EUSPIRA FORTUNEI
Figure 2. Calliper measurements on Euspira fortunei and Ruditapes philippinarum used in this study. Abbreviations: H, shell height; W, shell width;
L, shell length.
Table 1. Setup information for experiments testing for the prey-size preference in Euspira fortunei.
Tank ID
Shell height of
Number of
predators (mm)
predators
Size of tank (cm)
Time interval examined
A
11 – 13
B
13 – 15
3
11.5 × 17.5 × 10.5
6 Oct. 2010 –4 Jan. 2011
2
11.5 × 17.5 × 10.5
C
6 Oct. 2010 –4 Jan. 2011
15 – 17
7
11.5 × 17.5 × 10.5
6 Oct. 2010 –4 Jan. 2011
D
17 – 19
6
11.5 × 17.5 × 10.5
21 Nov. 2010 – 19 Feb. 2011
E
19 – 21
5
11.5 × 17.5 × 10.5
21 Nov. 2010 – 19 Feb. 2011
F
21 – 23
3
11.5 × 17.5 × 10.5
21 Nov. 2010 – 19 Feb. 2011
G
23 – 25
2
11.5 × 17.5 × 10.5
21 Nov. 2010 – 19 Feb. 2011
H
25 – 27
3
11.5 × 17.5 × 10.5
6 Oct. 2010 –4 Jan. 2011
I
27 – 29
4
11.5 × 17.5 × 10.5
6 Oct. 2010 –4 Jan. 2011
J
29 – 31
5
11.5 × 17.5 × 10.5
6 Oct. 2010 –4 Jan. 2011
K
31 – 33
4
14.0 × 22.0 × 12.0
6 Oct. 2010 –4 Jan. 2011
Figure 3. Zones used for categorizing the locations (sites 1– 9) of drillholes produced by Euspira fortunei on the shells of Ruditapes philippinarum (after
Kelley, 1988).
drillhole diameters (outer drillhole diameter: ODD; inner drillhole diameter: IDD) were measured to the nearest 0.01 and
0.001 mm using a digital calliper and a microscope (VH-5500,
Zoom Lens VH-Z20R, 30 –50 magnification), respectively.
Observations were performed at least once per week.
and low-competitive predation environments. In the highcompetition environment, 43 predators of similar sizes (mean
shell height + SD ¼ 21.40 + 3.13 mm) and 6 prey clams (shell
length: 20 –25 cm) were introduced to a glass tank (30 25 cm, 20 cm high) with filtered running seawater. The glass
tank was partially filled with a 5-cm layer of coarse sand.
Observations were performed once every 2 d. If the predators
consumed the clams, the same number of clams was added to
the tank to maintain a constant number of available prey (i.e.
six clams). This experiment was conducted between 6 October
and 20 November 2010. In the low-competition environment,
Comparison of drillhole locations for environments with high
and low competition
To test how one or multiple conspecific competitors influence
the shell-drilling behaviour of E. fortunei, we established high207
T. CHIBA AND S. SATO
Table 2. Summary of experiments testing for the prey-size preference in Euspira fortunei.
Shell height
of predators
(mm)
Shell length of prey (mm)
0– 5
5– 10
P
10 –15
15 – 20
20 – 25
25 –30
30 – 35
11 –13
2
4
4
3
1
0
0
,0.01
13 –15
2
4
4
4
4
1
0
,0.01
15 –17
0
4
4
4
4
4
1
17 –19
0
3
4
4
4
4
4
19 –21
2
4
4
4
4
4
4
0.15
21 –23
0
1
4
4
4
4
1
,0.01
23 –25
0
0
3
4
2
4
1
,0.01
25 –27
0
1
4
4
4
4
4
,0.01
27 –29
0
0
3
4
4
4
4
,0.01
29 –31
0
1
4
4
4
4
4
,0.01
31 –33
0
1
3
4
4
4
4
,0.01
Total
6
23
41
43
39
37
27
,0.01
0.017
,0.01
At the beginning of the experiments, seven sizes of Ruditapes philippinarum were offered as prey. Numbers of prey consumed by E. fortunei during the 90-d
experiments are presented.
we isolated 27 similarly sized predators (mean shell height +
SD ¼ 23.58 + 6.39 mm) into 27 separate plastic tanks (5.7 8.2 cm, 10.5 cm high) with several clams each. Observations
were performed at least once per week between 6 June and 6
July 2010. The drillhole locations on both the right and left
valves were categorized using the zones shown in Figure 3.
sediment leaving incomplete drillholes (Fig. 4C). In only one
successful attack, a copious amount of mucus was secreted by
the predator, which enveloped and probably helped immobilize the prey (Fig. 4D–F; Hasegawa & Sato, 2009).
When predators handled prey of their preferred size classes,
they selected highly stereotypical drillhole sites, whereas handling of very small or large prey relative to their preferred size
classes tended to result in abnormal drillhole placement
(Table 3; Fig. 5; Supplementary material). Prey/predator size
ratios ranged from 0.24 to 1.91. When the ratio is nearly equal
to one, sizes of predator and prey are matched; mismatch
occurs when the ratio deviates from one. Therefore, the data
were arbitrary divided into two groups based on the ratio (sizematched group: prey/predator size ratio ¼ 0.50–1.50; sizemismatched group: prey/predator size ratio ¼ 0.24 –0.50,
1.50– 1.91; Supplementary material). When each drillhole-site
category was merged into three groups (site 2, site 5, other
sites), a significant difference in drillhole sites was noted
between the two groups (Fisher’s exact test, P , 0.01;
Table 3). Drillhole sites in the former group were more stereotypical than those in the latter group, although the concentration of drillholes on site 2 was significant in both groups
(binomial test, P , 0.01; Table 3).
RESULTS
Prey-size preference and handling mechanics
To maintain statistically reasonable sample sizes, size categories of prey were merged into three groups (i.e. 0–10, 10–25
and 25– 35 mm). Fisher’s exact test rejected the null hypothesis
that the three groups have equal probability of being attacked,
with the exception of predators in the 19–21 mm size range
(Table 2). In addition, as predator size increased, the selected
prey size increased (Table 2). The smallest predators (shell
height 11 –13 mm) mainly fed on small clams (shell length
0–20 mm) and fed most frequently on clams in the 5 –15 mm
size range (Table 2). A total of 216 Ruditapes philippinarum were
consumed by Euspira fortunei during experiments over 90 d.
Medium-sized clams (10 –25 mm) were consumed by a wider
size range of predators than small (0–10 mm) and large
(25– 35 mm) clams (chi-square test, x 2 ¼ 91.83, df ¼ 2, P ,
0.01; Table 2).
The predators attacked their preferred prey-size classes in
the early stages of the experiments (Supplementary material).
When the preferred prey size became scarce due to predation,
some predators began to feed on relatively smaller or larger
prey, which had previously been ignored (Supplementary material, Appendix S1). For example, predators in the 13 –15 and
17– 19 mm size ranges ate clams that were between 5 and
20 mm during the early stages of the experiments
(Supplementary material, Appendix S1B, D). When clams
between 5 and 20 mm became scarce, the predators began to
feed on clams that were between 20 and 30 mm
(Supplementary material, Appendix S1B, D).
When predators handled individuals of their preferred preysize classes, they could firmly envelop the clams (Fig. 4B).
However, predators could not firmly envelop the clams when
these were very small or large relative to their preferred size
(Fig. 4A, C). We observed that predators in the 15– 17 mm
size range attacked unusually large clams (30 –35 mm) on
three occasions, but two of the three attacks failed to subdue
the clams and the predators then burrowed back into the
Relationship between predator size and drillhole diameters
The ODD and IDD values were significantly correlated with
the shell heights of E. fortunei; the Pearson’s correlation coefficient was more robust for the ODD correlation (r ¼ 0.984, P ,
0.01; r ¼ 0.968, P , 0.01 respectively; Fig. 6). The relationships between predator size and drillhole sizes (ODD and
IDD) were described by the following equations:
Outer drillhole diameter ðmmÞ ¼ 0:0927 shell height
þ 0:3830 mm
Inner drillhole diameter ðmmÞ ¼ 0:0573 shell height
þ 0:2303 mm
The drillholes produced by E. fortunei showed a characteristic
countersunk profile that did not change with the predator size
(Figs 5, 6).
208
STEREOTYPICAL PREDATION IN EUSPIRA FORTUNEI
Figure 4. Stereotypical predatory behaviour of Euspira fortunei. A. When a predator attacked a clam that was small relative to its preferred size
range, the predator could not fully envelop the clam. Prey/predator size ratio ¼ 10.91/22 ¼ 0.49. B. When a predator attacked certain preferred size
classes of clams, the predator could fully envelop the prey. Prey/predator size ratio ¼ 21.54/22 ¼ 0.97. C. When a predator attacked a clam that was
large relative to its preferred size range, the predator could not fully envelop the prey. Note that an incomplete drillhole was left around the umbo
of the clam. Prey/predator size ratio ¼ 30.52/16 ¼ 1.90. D –F. A series of predatory behaviours for preying on a clam that is larger than the
predator’s preferred size range. Prey/predator size ratio ¼ 30.52/16 ¼ 1.90. D, E. The predator attacked the clam, but the foot and siphons of the
clam interfered with the predatory behaviour. F. The predator secreted copious mucus and immobilized the clam.
Table 3. Comparison of drillhole sites for the size-matched and size-mismatched prey.
Group
Drillhole site
Site 1
Site 2
Site 3
Site 4
Site 5
Site 6
Site 7
Site 8
Site 9
Total
Size-matched
0
158
0
0
1
0
0
2
0
161
Size-mismatched
0
43
0
1
5
0
2
5
0
55
Data were divided into two groups named the size-matched ( prey/predator size ratio ¼ 0.50 – 1.50) and size-mismatched ( prey/predator size ratio ¼ 0.24 – 0.50,
1.50 – 1.91) groups.
Figure 5. Predatory drillholes produced by Euspira fortunei on shell of Ruditapes philippinarum. Note that all drillholes are countersunk. A. Prey/
predator size ratio ¼ 32.51/28 ¼ 1.16. The drillhole is located at site 2 (see Fig. 3). B. Enlargement of the drillhole in A. Outer drillhole diameter
(ODD) ¼ 3.41 mm. Inner drillhole diameter (IDD) ¼ 1.86 mm. C. Prey/predator size ratio ¼ 30.32/18 ¼ 1.68. The drillhole is located at site
7. D. Prey/predator size ratio ¼ 9.59/30 ¼ 0.32. The drillhole is located at site 5.
209
T. CHIBA AND S. SATO
on prey that were very small or large relative to their preferred
size (Fig. 4A, C). In addition, we observed that predators in
the 15–17 mm size range attacked unusually large clams (30 –
35 mm) on three occasions, in two of which the attacks failed
to subdue the clams. These observations suggest that it is difficult for predators to manipulate very small or large prey compared to their foot size, because of their stereotypical predatory
behaviour. As predators increase in size, the prey-size classes
that they can manipulate become larger.
Within the manipulation limits, predators may initially
select optimally sized prey, which maximizes their net rate
of energy intake. Predators selected their specific preferred
prey-size classes in the early stages of the experiments
(Supplementary material). After their preferred prey-size
classes became scarce due to predation, some predators began
to feed on relatively small or large prey, which had previously
been ignored. These results imply that E. fortunei has the
ability to assess the size of the prey, probably by feeling with
its foot. Dietl & Alexander (1997) argued that naticid predators attacked optimally sized prey when such prey were abundant, but prey with a less optimal size may be included in
their diet if they were unable to consume optimally sized prey
as expected based on optimal foraging theory (see Hughes,
1980). The present study implied that such a predator–prey
size mismatch is possible, although not all predators attacked
prey of a less optimal size when optimally sized prey became
scarce in our laboratory experiments.
Medium-sized clams (shell length range 10–25 mm) were
consumed by a wide size range of predators (Table 2). In contrast, small clams (shell length range 0–10 mm) were less susceptible to predation by E. fortunei in the 11 –33 mm size range
(Table 2). Sakai & Suto (2005) confirmed that juvenile E. fortunei (shell width range 1.2 –1.6 mm; Fig. 2) fed on juvenile
Ruditapes philippinarum (shell height range 0.8 –2.0 mm; Fig. 2).
It is probable that E. fortunei that are ,11 mm in shell height
are mainly responsible for the predation of small R. philippinarum (shell length range 0–10 mm). These results indicate
that there is no size refuge for R. philippinarum (shell length
range 0–35 mm) from attack by E. fortunei. Naticid predation
appears to be more intense for a certain size range of prey
(Edwards & Huebner, 1977; Wiltse, 1980b; Kingsley-Smith
et al., 2003). As a result, size-selective predation in naticids potentially influences the size-frequency distribution of prey
(Franz, 1977; Commito, 1982). It is also likely that the preferred size range of R. philippinarum (shell length range 10 –
25 mm) dramatically decreases in number due to the selectivity
of predation by E. fortunei. The preferred prey-size classes for
naticids are smaller than those for human consumption
(.25 mm in shell length). Local fishermen scatter juvenile
clams on tidal flats and harvest them after they have grown.
But the clams may be almost consumed before they grow to
marketable size because of the concentration of naticid predation. It is probable that the introduction of E. fortunei caused
significant loss in aquaculture, particularly of R. philippinarum
stocks.
The present study showed significant correlations between
the shell height of E. fortunei and both the inner and outer diameters of drillholes (Fig. 6). Similar relationships between
Comparison of drillhole sites in environments with high
and low competition
When the drillhole-site categories were merged into three
groups (site 2, site 5, other sites), no significant difference in
the drillhole sites was noted between the environments with
high and low competition (Fisher’s exact test, P ¼ 0.43;
Table 4). In the environment with high competition 73 clams
(mean shell length + SD ¼ 22.39 + 1.66 mm) were consumed
during the experiment. We found no evidence of cannibalism
in the high-competition tank. In the low-competition environment, 66 clams (mean shell length + SD ¼ 20.86 + 6.01 mm)
were consumed. All clams that were consumed by E. fortunei in
both environments were size-matched prey. In both environments, the concentration of drillholes on site 2 was significant
(binomial test, P , 0.01; Table 4) and predators never drilled
at the thin valve edge of the prey’s shell.
DISCUSSION
Size-selective predation and its potential impact
on prey population
In our laboratory experiments, Euspira fortunei was a sizeselective predator: there was a positive correlation between
predator and prey size (Table 2). It is well established that
naticids select larger prey as they increase in size, because the
prey-size limits are determined by the size of their foot, which
is the organ used for capturing and handling prey (e.g. Ansell,
1960; Edwards & Huebner, 1977; Griffiths, 1981; Rodrigues,
Nojima & Kikuchi, 1987; Kingsley-Smith, Richardson & Seed,
2003). It was confirmed that E. fortunei capture and handle
prey using the foot in the same manner as other naticids
(Hasegawa & Sato, 2009). The present study also showed that
predators could firmly envelop prey of their preferential size
(Fig. 4B), but they could not do this when they tried to feed
Figure 6. Linear relationships between predator size (shell height; see
Fig. 2) and drillhole diameters (outer drillhole diameter: ODD; inner
drillhole diameter: IDD) produced by Euspira fortunei on shells of
Ruditapes philippinarum. Black and white circles denote ODD and IDD,
respectively. n is the total number of drillholes examined.
Table 4. Comparison of drillhole sites for high- and low-competitive environments.
Competition for prey
Drillhole site
Site 1
Site 2
Site 3
Site 4
Site 5
Site 6
Site 7
Site 8
Site 9
Total
High
0
70
0
0
2
0
0
1
0
73
Low
0
66
0
0
4
0
0
0
0
70
210
STEREOTYPICAL PREDATION IN EUSPIRA FORTUNEI
predator size and drillhole diameters have also been shown for
other naticid species (Wiltse, 1980b; Griffiths, 1981; Kitchell
et al., 1981; Rodrigues, 1986; Hirayama et al., 1996;
Kingsley-Smith et al., 2003). Using this relationship, the preysize selectivity in natural settings can be estimated based on
drillholes on prey valves (e.g. Dietl & Alexander, 1997). Our
results therefore provide the opportunity to examine whether
E. fortunei is also a size-selective predator in natural settings.
Similarly, Amano (2006) argued that edge-drilled shells of
Glycymeris yesoensis produced by naticids might be evidence of
high competition for prey in the Japan Sea during the
Pleistocene. However, the present study suggests that intense
competition for prey does not always cause the drillhole site to
shift to the shell edge.
SUPPLEMENTARY MATERIAL
Supplementary material is available at Journal of Molluscan
Studies online.
The mechanics of selecting drillhole sites and the cause
of anomalous drillhole placement
ACKNOWLEDGEMENTS
When predators handled size-matched prey, the drillhole sites
were highly stereotypical. However, they tended to drill abnormal sites when handling size-mismatched prey (Table 3;
Fig. 5). The anomalous placement of drillholes by naticids
commonly occurs in size-mismatched prey (Negus, 1975;
Kitchell et al., 1981; Bayliss, 1986). As summarized by Kabat
(1990), drillhole placement is primarily a function of the
manipulation of the prey during drilling and may depend on
the shell morphology of the prey. As described in this study,
E. fortunei could not firmly envelop prey that were very small
or large compared to its foot size. As a result, E. fortunei was
forced to drill such size-mismatched prey in an abnormal
posture (Fig. 4A, C); therefore, drillholes tended to be located
in anomalous sites. It is possible that a less stereotypical placement of drillhole by naticids is the result of the scarcity of specific preferred prey-size classes and consequent attacks on
size-mismatched prey.
The drillhole sites selected by E. fortunei were highly stereotypical regardless of competition for prey (Table 4) and they
never drilled at the thin valve edge of the prey’s shell.
Edge-drilling is a faster but riskier predatory behavior, because
a prey clam can damage the feeding organ ( proboscis) by
clamping down (Dietl & Herbert, 2005). Therefore, in
Chicoreus dilectus (Muricidae), edge-drilling of prey bivalves
(Chione elevata) was avoided when competition was reduced,
whereas edge-drilling was used when competition was intense
(Dietl et al., 2004). However, such alternative predatory behaviour was not observed in the present study despite the presence
of competitors. This result may not be surprising, since edgedrilling has not been reported in Euspira (G.P. Dietl, personal
communication). Edge-drilling has, however, been observed in
some naticids, which typically live in tropical to subtropical
regions, despite low-competitive settings (Vermeij, 1980; Ansell
& Morton, 1987). Further investigations are needed to elucidate the relationship between edge-drilling and competition.
Some significant differences in predatory behaviour between
naticids and muricids may be noteworthy. It is likely that naticids are less likely to be disturbed by competitors than muricids, because naticids commonly consume prey within the
substrate. On the other hand, muricids commonly consume
prey on the substrate or rock surface, where the likelihood of
being disturbed by competitors may be greater. Therefore, the
risks from competitors while drilling bivalve prey might be a
less important determinant of fitness in the case of naticids. In
addition, naticids may have less flexibility in drillhole placement, because they handle prey in stereotypical posture. On
the other hand, muricids crawl across bivalve prey before beginning to drill, and thus may have more flexibility in drillhole
position.
Although our inference here is speculative, it has implications for the interpretation of edge-drilled valves in both extant
and fossil assemblages. Dietl et al. (2004) considered the relatively high proportion of edge-drilled shells of C. elevata produced by C. dilectus in the western Atlantic region during the
Pliocene to be the result of intense competition for prey.
We thank H. Kano (Tohoku University Museum) for his instruction in microscope use. We also thank O. Sasaki (Tohoku
University Museum) and K. Okoshi (Toho University) for
valuable discussions. We are grateful to E. Boulding, M. Grey
and G.P. Dietl for their critical comments and useful suggestions that have helped to improve our paper.
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