Forgot your password?
Document Actions
watanabe
Marine Biology (2006) 148: 1021–1029
DOI 10.1007/s00227-005-0152-9
R ES E AR C H A RT I C L E
Jeffrey T. Watanabe Æ Craig M. Young
Feeding habits and phenotypic changes in proboscis length
in the southern oyster drill, Stramonita haemastoma
(Gastropoda: Muricidae), on Florida sabellariid worm reefs
Received: 2 May 2005 / Accepted: 22 September 2005 / Published online: 15 November 2005
Ó Springer-Verlag 2005
attacks and consumes worms in 15–50 min. In the lab-
Abstract The southern oyster drill, Stramonita (= Thais,
oratory, oyster drills consumed 1.7 worms per day,
Kool 1987) haemastoma, is a common intertidal and
spending <1 h each day feeding. On sabellariid reefs,
subtidal predator in the southeastern United States. It
differences in feeding, handling costs, and prey value, are
uses specialized feeding structures and foraging strate-
likely to have a significant effect on the ecology and life
gies to bore holes through the shell of its bivalve prey.
history of S. haemastoma in this habitat.
However, on the east coast of Florida, S. haemastoma, is
common on sabellariid worm reefs constructed by the
polychaete Phragmatopoma lapidosa (Walton Rocks
Beach, Florida, 27°17¢N, 80°12¢W), a habitat where the
snail’s typical prey are scarce. From 1999 to 2001, we Introduction
examined the feeding habits of S. haemastoma on sab-
ellariid reefs and the behavioral and morphological Many predators exhibit specialized foraging strategies
responses of S. haemastoma that accompanied switching and morphological adaptations that have arisen in re-
from a diet of bivalves to sabellariids. On worm reefs sponse to selective pressures imposed by specific types of
S. haemastoma feeds on P. lapidosa by inserting the prey (Schoener 1971). Shell-boring in gastropods is a
proboscis deep into a worm’s tube. Worm-feeding snails feeding strategy that permits some snails to feed on
had longer proboscises ($3.7 times shell height) than bivalves and other shelled benthic invertebrates— prey
bivalve-feeding conspecifics ($2.0 times shell height). whose defenses present significant challenges to attack-
Snails raised on different diets showed significant dif- ers. To circumvent these defenses, shell-boring gastro-
ferences in proboscis length suggesting that the pro- pods drill a hole through the calcareous shell of their
boscis length is phenotypically plastic. Whereas typical prey using a combination of radular scraping and
oyster drills must bore holes for days before ingesting chemical dissolution. An accessory boring organ secretes
prey, S. haemastoma on worm reefs avoids boring and enzymes intermittently, which helps soften and dissolve
the area being drilled (Carriker 1978, 1981). After a hole
is made in the shell, a long proboscis extends into the
Communicated by J.P.Grassle, New Brunswick shell and the soft tissue is torn off and ingested. Thus,
the ability to bore through shell and then feed on its
J. T. Watanabe
contents required the evolution of several anatomical,
Harbor Branch Oceanographic Institution,
5600 US 1 North, Ft, Pierce, FL 34946, USA physiological, and behavioral innovations.
Feeding on an individual shelled prey item may take
C. M. Young
several hours to several days, requiring a substantial
Florida Institute of Technology, Melbourne,
commitment of both time and energy. The significant
150 W. University Blvd, Melbourne, FL 32901, USA
handling costs associated with shelled prey have led to
Present address: J. T. Watanabe (&) the evolution of foraging strategies that reduce handling
Department of Biology, Ohlone College,
time and other costs, and maximize energy intake
Fremont, CA 94539, USA
(Hughes 1980). When given a choice, shell-boring snails
E-mail: jwatanabe@ohlone.edu
tend to select prey of optimal size and will choose more
Tel.: +1-510-6596000
Fax: +1-510-6596244 easily accessible or energetically rich species of prey over
others (Garton 1986; Brown and Richardson 1987;
C. M. Young
Brown 1997). Feeding behaviors such as attacking the
Oregon Institute of Marine Biology,
margin or lip of shells where defenses are weakest
Charleston, OR 97420, USA
1022
canaliculata-like are more common along the Gulf coast
(Gunter 1979), or foraging in groups (Brown and Alex-
of Louisiana, Mississippi, and Florida, while floridana-
ander 1994) save time and energy. Some larger oyster
like snails are more prevalent in Texas and at two sites
drills may avoid boring altogether by secreting a toxin
on the Atlantic coast of Florida. However, the same
that causes bivalves to gape (McGraw and Gunter 1972).
study found that genetic differences did not correlate
Given the specialized nature of their feeding struc-
with differences in shell or radular morphology, char-
tures and foraging habits, shell-boring gastropods often
acteristics previously used to differentiate the subspecies.
occur where bivalves and other shelled prey are abun-
In this study, we collected bivalve-feeding S. haemas-
dant. In the southeastern United States, the southern
toma from a site on the Atlantic coast of Florida where
oyster drill, Stramonita haemastoma, feeds on the eastern
Liu et al. (1991) found 114/128 floridana-like snails, 7/
oyster, Crassostrea virginica (reviewed by Butler 1985),
128 canaliculata-like, and 7/128 possible hybrids.
mussels, Ischadium recurvum, and clams Rangia cuneata
Unfortunately, no genetic analyses have been conducted
(Brown and Richardson 1987). In the Florida Keys, they
on sabellariid reef populations of S. haemastoma where
feed on two species of tree oysters, Isognomon bicolor
our other snails were collected. In the absence of any
and I. radiatus, the mussel Brachidontes exustus, and the
information to the contrary, we assume that snails from
barnacle Tetraclita squamosa (Ingham and Zishke 1977).
both our study sites belong to the subspecies floridana.
They also attack the bivalves Donax variabilis, Perna
Other than allozyme differences revealed by Liu et al.
perna, Anomia simplex, Mercenaria mercenaria, and the
(1991), no significant biological differences between the
gastropod Crepidula plana and cannibalize smaller con-
subspecies have been established.
specifics (Butler 1985).
However, on the Atlantic coast of Florida, popula-
tions of S. haemastoma occur on sabellariid worm reefs,
Materials and methods
a habitat where large populations of bivalve prey are
unavailable to them. Sabellariid reefs are formed by
Study sites
large aggregations of the tube-building polychaete
Phragmatopoma lapidosa (Sabellariidae). Huge intertidal
Stramonita (= Thais, Kool 1987) haemastoma were
and subtidal mounds consisting of thousands of sand
collected from two sites on the east coast of Florida,
tubes form reefs, and each mound may cover several
USA, between 1999 and 2001. Walton Rocks Beach
square meters (Kirtley 1968). We witnessed S. haemas-
(27°17¢N, 80°12¢W) (WR) is located on the ocean side of
toma living directly on the worm mounds and sheltering
a barrier island, approximately 65 km north of Palm
in the cracks and crevices of the reef when not feeding.
Beach, Florida. A sandy beach slopes into the sea where
On sabellariid reefs, oyster drills feed primarily on P.
scattered limestone coquina foundations support
lapidosa. For a predator that specializes on bivalves,
mounds of intertidal and subtidal P. lapidosa worm reef.
switching to a diet of tubeworms is a major shift in
Snails <25 mm in shell height were collected at low tide
foraging strategy. Differences in prey defense also pres-
primarily between the months of November and Feb-
ent challenges that must be overcome for S. haemastoma
ruary. Clumps of worm tubes were collected regularly to
to survive on sabellariid reefs.
feed the snails and for use in experiments. Both worms
Stramonita haemastoma is considered a pest of the
and snails were transported in buckets of seawater to
commercial oyster industry and as a result, its feeding
our laboratory at Harbor Branch Oceanographic Insti-
habits on oysters and on other bivalves have been
tution (HBOI) where they were maintained in aquaria at
extensively studied (review by Butler 1985). However, no
room temperature ($23°C).
information exists on the feeding habits of S. haemas-
Stramonita haemastoma from WR were compared
toma on P. lapidosa worm reefs. We examined feeding
with snails at Marineland, Florida (29°40¢N, 81°12¢W)
behavior, feeding rate, and handling time of S. ha-
(ML), approximately 270 km further north. At this site,
emastoma feeding on P. lapidosa tubeworms. The long
snails occur on intertidal limestone boulders that form
proboscis of S. haemastoma is its most functionally
groins perpendicular to the beach. Wave action and sand
important feeding structure on worm reefs, so we com-
surrounding the boulders probably prevents emigration
pared the proboscises of worm predators with those of
from the study site. P. lapidosa does not occur at this site
bivalve predators from another habitat to see if differ-
and snails were found feeding on the small ($7 mm)
ences in habitat and prey were correlated with proboscis
bivalve Lyonsia hyalina and the barnacle Balanus
length. Finally, snails from different habitats were
amphitrite which occurs slightly higher in the intertidal.
maintained on diets of worms or bivalves to determine if
Snails of shell height 20–35 mm were collected at low tide
changes in proboscis length are inducible.
and transported in buckets of seawater to the laboratory.
In the southeast United States, two subspecies, S.
We measured shells with vernier calipers to the nearest
haemastoma canaliculata (Gray 1839) and S. haemas-
0.1 mm from the siphon to the tip of the spire. Prior to
toma floridana (Conrad 1837) have been described based
the experiments, WR snails were maintained on a diet of
on differences in shell and radular morphology. A
P. lapidosa. Because the bivalve Lyonsia hyalina, was not
population genetics study of snails in this region iden-
readily available near the laboratory, ML snails were fed
tified two genetically differentiated groups of S. ha-
the oyster C. virginica, collected from a nearby seawall.
emastoma (Liu et al. 1991). Snails characterized as
1023
60
50
Time (min)
40
30
20
10
24 26 28 30 32 34 36 38 40
Shell Height (mm)
Fig. 2 Stramonita haemastoma. Relationship between shell height
and time to consume a single P. lapidosa in a synthetic tube (n =
12, y = 0.938x + 63.575, r2 = 0.208)
Fig. 1 Stramonita haemastoma. Attack on Phragmatopoma lapid-
pipettes (Fig. 1b). Six tubes (interior diameter 3 mm)
osa in a A sand tube constructed by P. lapidosa on plexiglass. b A
were mounted and glued in a frame of two 15·20 cm2
1-ml plastic pipette (Photo W. Tyler). Time-lapse video and lines on
acrylic sheets. The sheets had holes to hold the tubes
pipette were used to measure length of snail proboscis. Arrow
indicates tip of snail’s proboscis. Scale bar 10 mm in place, which were spaced two per row, with open-
ings mounted flush with one sheet. Six tubes were used
to increase the likelihood that a snail would encounter
Feeding behavior, handling time, and proboscis length
a worm. Individual worms were removed from their
sand tubes and placed inside the pipettes, posterior
Stramonita haemastoma attack and consume P. lapidosa
end first, with the head towards the opening of the
within the worm tubes, making it difficult to observe
pipette. Three or four snails at a time were labeled
feeding. We, therefore, developed two new methods to
with nail polish and introduced to a 15-l seawater
observe the feeding behavior of S. haemastoma on P.
aquarium containing the pipettes and worms. Using a
lapidosa. Individual tubeworms were cultured on trans-
Panasonic time-lapse video recorder, we videotaped
parent acrylic sheets and encouraged to build natural
the aquarium for 72 h to observe feeding behavior
sand tubes on the transparent surface (Fig. 1a). A sim-
over extended periods of time. As snails fed, they
ilar technique was previously used to observe the
extended their proboscis down the tube, and the
behavior of P. lapidosa within sand tubes (J. Pawlik,
worms either retreated or were pushed by the pro-
personal communication). We broke apart clumps of
boscis. As the worms retreated, S. haemastoma,
worm reef and isolated individual P. lapidosa within
their sand tubes. Each tube was shortened to $15 mm, extended its proboscis further. Markings on the tube
visible in the video replay enabled measurement of
making the tubes approximately the same size as the
worms, and placed them on 10·10 cm2 clear acrylic proboscis length. Whenever possible, handling time
(the time from initial proboscis extension until the
sheets in an aerated seawater aquarium. The remaining
worm was consumed) was recorded from video foot-
tube fragments were crushed into individual sand grains.
age or real-time observations. The aquarium was near
A trail of sand was placed in front of each worm tube.
a window and so natural light and dark cycles existed
When left undisturbed for 2–3 weeks, the worms
during the duration of the experiment.
reconstructed tubes on the acrylic sheet. This created an
We compared the proboscis lengths of snails from the
‘ant farm’ effect that allowed a view of the worm within
WR and ML sites to determine if different types of
the tube. During tube building, worms were fed the
available prey (and the different methods of handling
diatom Chaetoceros gracilis. Stramonita haemastoma
these prey) were related to proboscis length. After each
was then placed with the worm and the sheet was in-
proboscis was measured, we removed the snail from the
verted under water. Under a dissecting microscope,
aquarium and measured shell height. Shell height to
feeding behavior was observed from above with the
proboscis length regressions were compared between
worm and snail on the opposite side of the clear sheet.
the two sites, using ANCOVA, with shell height as a
Snail feeding behavior was also observed in artifi-
covariate to eliminate the effects of snail size.
cial tubes made from 1-ml clear graduated plastic
1024
Phenotypic plasticity determine the number consumed by the snail. Feeding
rate (worms per day) was calculated as the number of
Stramonita haemastoma feeding on worms had much worms consumed during the experiment, divided by
longer proboscises than snails feeding on oysters. To days of the study.
determine if proboscis length changes phenotypically
with a change in diet, we maintained separate groups of
Phragmatopoma lapidosa tissue dry-mass
snails from WR and ML on diets of either C. virginica
($65 mm from hinge to posterior shell edge) or P. lap-
To determine the amount of tissue consumed by the
idosa. At the beginning of the experiment, snails from
snails, we calculated the average dry tissue weight of
WR were slightly smaller (22.8±2.4 mm) than those
individual P. lapidosa collected at WR in April 2001.
from ML (26.3±3.2 mm). Snails of this size range have
One hundred worms were removed from their tubes and
not yet attained reproductive maturity and were re-
fixed in 10% formalin and sea water. Body length of
cruited within 6 months of collection (unpublished).
each worm was measured to the nearest 0.01 mm from a
Stramonita haemastoma may attain shell heights of
digital photograph, using University of Texas Health
>100 mm and live for several years and have been
Science Center San Antonio (UTHSCS1A) imaging
known to grow 25 mm in just 30 days in the laboratory
program version 2.0. Undamaged worms (n=41) were
(Butler 1987).
then oven-dried at 60°C for 24 h and weighed on a
Snails were maintained in five, 47-l aquaria, each di-
vided into 12, 12 · 6 · 14 cm3 chambers. Snails were Mettler AE 163 analytical balance. After total body
weight was measured, the operculum was removed from
paired within chambers because the experiment also
the worm and weighed to determine the percentage of
measured reproductive output (Watanabe 2002). Each
worm mass attributable to the operculum, the only part
tank had six snails from each habitat fed with each type
of the worm that is not consumed by the snail.
of prey. Each chamber received either one clump of
The dry tissue consumed per day was calculated by
Phragmatopoma lapidosa (>200 individuals) every
multiplying the number of worms eaten per day from the
4 weeks, or one cracked C. virginica oyster every 10–
feeding experiment by the average dry tissue weight
14 days. Oysters were cracked open with a hammer so
without the operculum. P. lapidosa spawns when stres-
that regular feeding intervals could be maintained and
sed, and dry mass did not account for missing mass due
feeding would not be delayed by individual differences in
to release of eggs or sperm when worms were originally
the timing of shell-boring. This method should not affect
removed from their tubes. When P. lapidosa are being
the way the proboscis is extended when feeding on
consumed by S. haemastoma, the worms may likely
oysters. A preliminary study showed no significant dif-
spawn before being eaten, and snails may not recover
ference in growth of snails that fed on opened or closed
that biomass anyway. This was not, however, observed
oysters (Watanabe 2002).
in our feeding experiments because worms released their
After 11 months, snails were removed from aquaria
gametes during the experimental setup prior to the
and proboscises were measured as described previously.
introduction of the snails. Phragmatopoma lapidosa are
Fifteen snails from each of the four site-prey combina-
capable of spawning the year round (McCarthy 2001),
tions were measured. Proboscis lengths were compared
but at WR settlement was heaviest in September and
using a two-way factorial ANCOVA with prey (fixed)
October and abundance declined by August (Watanabe
and site (random) as the factors and shell height as the
2002).
covariate.
Profitability of prey, (Brown and Richardson 1987),
was calculated as the amount of dry tissue consumed per
hour of feeding effort. The mean dry mass of P. lapidosa
Feeding rate
(without the operculum) was divided by the mean time it
took snails to consume a single worm (as determined by
We estimated feeding rate of S. haemastoma on P. lap-
the handling time studies). This yielded the amount of
idosa in an experiment in April 2001. We put S. ha-
dry tissue consumed per hour of handling time.
emastoma (mean shell height 23.3±0.8 mm) in 11
replicate, 2-l plastic containers of aerated seawater with
clumps of worm reef (11–15 worms clumpÀ1) for 7 days.
Results
Three 2-l containers holding only worm clumps were
used as controls. Prior to the experiment, all snails were
Feeding behavior and handling time
kept in tanks with an ample supply of P. lapidosa
clumps. After 7 days, the remaining worms were coun-
After S. haemastoma were placed in tanks containing P.
ted to determine the number of worms consumed. Half
lapidosa, the snails either searched for prey, or became
the water in each container was replaced twice during
inactive and did not move for some time. Videotaped
the experiment and all containers were kept at room
observations over 72 h showed an apparently random
temperature ($23 C). After 7 days, worm clumps were
activity pattern that did not correlate with any diurnal
broken apart and the number of worms remaining in
or tidal patterns.
each replicate was subtracted from the initial number to
1025
Like other predatory gastropods, S. haemastoma 180
made lateral movements of the siphon while searching 160
for prey, presumably testing the water from different
Proboscis Length (mm)
140
directions. Snails found the opening of the worm tubes
120
with their siphons, often touching the tentacles of
P. lapidosa in the process. The worms retracted upon 100
contact but generally did not retreat down their tubes 80
immediately. Snails initiated feeding by covering the 60
external opening of the worm tube with the anterior
40
portion of the foot. The snails then inserted their Walton Rocks
20
proboscises into the opening of the tube. When the Marineland
proboscises touched the tentacles or chitinous opercu- 0
lum of P. lapidosa, the worms retreated into the tube. 22 24 26 28 30 32 34 36 38 40 42 44
Shell Height (mm)
The snails followed the worms with their proboscises,
rasping with their radula in an apparent attempt to
Fig. 3 Stramonita haemastoma. Relationship between shell height
slow down or capture the retreating worm. P. lapidosa and proboscis length for snails from two populations with different
was captured when it could not retreat any deeper, or prey (n = 19 for each). Shell height was not a good predictor of
proboscis length for snails from WR (y = 0.458x + 106.795, r2 =
when the radula of S. haemastoma caught the opercular
0.010) nor snails from ML (y = 1.839x + 3.695, r2 = 0.477).
plate of the worm. The operculum was slightly smaller
Proboscises of snails preying on P. lapidosa predators from WR
than the diameter of the tube and allowed movement were significantly longer than bivalve predators from ML (Table 1)
of the worm up or down the tube while keeping the
head of the worm covered. S. haemastoma scraped at
the operculum until it tilted to one side, rendering the
Proboscis length
soft head of P. lapidosa vulnerable to attack. Once the
soft tissue was accessed, S. haemastoma tore bits of
Stramonita haemastoma from WR that fed on P.
flesh from its prey. In the tube, some snails slowly
lapidosa had much longer proboscises than conspecifics
retracted the proboscis as they fed, pulling the worm
from ML that fed on bivalves (Fig. 3, Table 1).
toward the opening of the tube. Near the tip of the
Differences in proboscis length varied with habitat
proboscis, microscopic particles of detritus and sand
and were not explained by differences in shell height.
moved rhythmically back and forth as the snail fed,
Individuals from WR 26.1 to 42.5 mm shell height had
suggesting a sucking or pumping force during feeding.
proboscises 85.1–159.6 mm long. Proboscis length was
When feeding on bivalves, the muscular proboscis
not significantly correlated with shell size; probos-
pumps liquefied oyster tissue from the shell of prey.
cises ranged from 2.34 to 5.46 times the height of the
In addition to bringing particles to the mouth, the
suction helped S. haemastoma slow down the retreat of
P. lapidosa and pulled the worm toward the proboscis.
S. haemastoma used two different methods of ingesting Table 1 Stramonita haemastoma ANCOVA table comparing the
effect of habitat on proboscis lengths with shell height as the co-
the remainder of the prey. In some cases, snails con-
variate
sumed the worms with the proboscis extended into the
tubes; in other cases, they pulled the worms to the Source of df SS MS F P
opening of the tube before ingestion. Tiny pieces of variation
tissue moved in rhythmic pulses down the length of the
Shell 1 984.46 984.46 3.01 0.091
semi-transparent proboscis. S. haemastoma ate all soft
Site 1 31,443.95 31,443.95 96.27 <0.001
parts of the polychaete but never consumed the chi- Error 35 11,431.33 326.61
tinous operculum. Total 37 47,533.87
Stramonita haemastoma rapidly attacked and con-
sumed individual P. lapidosa when compared to other
types of prey. Feeding times on P. lapidosa ranged Table 2 Stramonita haemastoma ANCOVA table comparing the
from 14 to 50 min. In 13 timed attacks in artificial tubes, effect of habitat and diet on proboscis lengths of snails with shell
S. haemastoma consumed P. lapidosa in a mean time of height as the covariate for groups of snails in the laboratory
32.2±8.3 (SD, range 14–50) min. In another study,
Source of df SS MS F P
similarly sized S. haemastoma took 20 h to feed on the
variation
mussel I. recurvum, and up to 70 h to consume clumped
C. virginica (Brown and Richardson 1987). Snails fed Shell 1 648.51 648.51 2.20 0.144
continuously once they began ingesting the tissue and Site 1 6.15 6.15 0.02 0.886
Prey 1 3,049.74 3,049.74 10.33 < 0.01
stopped only after all soft tissue was eaten. The size of
Site · Prey 1 913.35 913.35 3.09 0.085
snails did not show a strong relationship with feeding
Error 55 16,237.43 295.23
time (Fig. 2). Profitability for snails feeding on worms Total 59 20,291.90
was 6.76 mg DW hÀ1 of handling time.
1026
140
P. lapidosa diet
Proboscis length / Shell height
Walton Rocks C. virginica diet
4
120
100 3
80
2
Proboscis Length (mm)
60
P. lapidosa
1
C. virginica
40
20 25 30 35 40 45 50 55 0
Marineland
Walton Rocks
140 Site
Marineland
120 Fig. 5 Stramonita haemastoma. Ratio of proboscis length to shell
height for snails from two different sites (WR and ML) maintained
for 9 months on diets of P. lapidosa or C. virginica. Error bars = 1
100
SD (n = 16 for each site-prey combination)
80
2.02±0.34 times shell height (Fig. 5). On a diet of
60
Phragmatopoma lapidosa, snails from ML had probos-
cises 3.21±0.76 times the height of the shell, whereas
40
snails from the same site fed oysters, had proboscises
20 25 30 35 40 45 50 55
only 1.97±0.38 times the shell height. By the end of the
Shell Height (mm) experiment, nearly all snails raised on oysters had larger
shells than snails fed P. lapidosa, irrespective of where
Fig. 4 Stramonita haemastoma. Relationship between shell height
the snails had originated.
and proboscis length from two different sites (WR and ML)
maintained for 9 months on diets of P. lapidosa or Crassostrea
virginica. Proboscises of snails fed P. lapidosa were proportionally
longer than those fed C. virginica (Table 2). Regressions indicate
Phragmatopoma lapidosa length and mass
that shell height was not a good predictor of proboscis length for
snails from WR maintained on P. lapidosa (y = 0.171x + 85.884,
r2 = 0.003) or on C. virginica (y = 0.336x + 99.745, r2 = 0.025) Phragmatopoma lapidosa collected in April 2001 had a
nor for snails from ML maintained on P. lapidosa (y = 0.387x + mean length of 14.55±2.92 mm (range 8.34–20.94) and
84.660, r2 = 0.01) or on C. virginica (y = 1.671x + 11.492, r2 = a dry mass of 4.233±1.584 mg mmÀ1 wormÀ1 (n = 41)
0.376)
(range 1.2–8.8 mg mmÀ1 wormÀ1). The average amount
of consumable tissue (without the operculum) was
snail’s shell (mean 3.74±0.85 SD). One individual 3.664±1.419 mg. The operculum of P. lapidosa made up
with a 28.7 mm shell had a proboscis 156.6 mm long.
Snails from ML 24.5 to 39.4 mm shell height had
proboscises 42.6–79.0 mm long. Proboscises ranged
from 1.44 to 2.67 times the height of their shells, with a 1.0 y = 1.368x -1.0489 r2 = 0.488
mean of 1.96±0.30 (SD) times shell height. Thus, snails
from WR that normally feed on worms can extend their 0.8
Log Weight (mg)
proboscises about 1.9 times further than snails from ML
that normally feed on bivalves. 0.6
Stramonita haemastoma maintained in the laboratory
for 11 months on a diet of P. lapidosa had significantly 0.4
longer proboscises than snails fed oysters irrespective of
0.2
size or original habitat (Fig. 4, Table 2). Regressions
indicate that shell height was not a good predictor of
0.0
proboscis length for snails from WR maintained on
P. lapidosa (y = 0.171x+85.884, r2 = 0.003) or on
C. virginica (y = 0.336x+99.745, r2 = 0.025), nor for 0.8 0.9 1.0 1.1 1.2 1.3 1.4
snails from ML maintained on P. lapidosa (y = 0.387x+ Log Length (mm)
84.660, r2 = 0.01) or on C. virginica (y = 1.671x+
11.492, r2 = 0.376). Fig. 6 Phragmatopoma lapidosa. Relationship between length and
dry mass of worms from WR in April 2001 (n = 41) All values were
Snails from WR fed tubeworms had proboscises log transformed and mass increased significantly with length.
2.62±0.73 times shell height, whereas snails from the Worm length increased with mass (y = 1.368x À1.0489, r2 =
same site fed C. virginica had shorter proboscises, 0.488)
1027
escape an attack. Using grains of sand, P. lapidosa
approximately 13.6±3.6% of the total dry mass of the
increases the length and diameter of its tube as it
worm. Dry mass of P. lapidosa was positively related to
matures. The most recently constructed part of the tube
worm length (Fig. 6).
is near the opening and is wider than older parts of the
tube which are built when the worm is smaller. Even
though sabellariid reefs may be >1 m tall, the length of
Feeding rate
tube occupied by the worm is much shorter, leaving
worms within reach of S. haemastoma. Worms could
Stramonita haemastoma consumed a total of 10.8±2.7
potentially respond to predation pressure by building
(SD) Phragmaopoma lapidosa in 7 days. Snails ate about
longer tubes, but this would create larger worm mounds
5 to 14 worms during the feeding period. Their mean
daily feeding rate was 1.57±0.38 worms snailÀ1 dayÀ1, that are less stable and more likely to break under wave
equivalent to 5.76±1.40 mg DW snailÀ1 dayÀ1. All pressure. Also, longer tubes in the intertidal might reach
above the water line and would increase exposure and
control worms remained alive during the duration of the
stress during low tide.
experiment. One snail that escaped from its tank and
At WR two non-shell-boring gastropods, Pollia tincta
died was not included in the measurements.
(Buccinidae) and Leucozonia nassa (Fasciolaridae), were
observed feeding on P. lapidosa with long proboscises
Discussion inserted in worm tubes, though these species were rare
compared to S. haemastoma. Decapod crustaceans
The feeding habits of S. haemastoma living on sabellariid (Gore et al. 1978) and S. haemastoma probably account
worm reefs differ from conspecifics in more typical for the greatest predation pressure on P. lapidosa where
habitats. Major differences in handling costs, prey de- they co-occur.
fense, and mode of feeding affect foraging on the reefs. Differences in proboscis length between snails
A diet of worms does not require snails to bore through collected from WR and ML are attributable to phe-
shell, drastically reducing the amount of time and energy notypic plasticity of the feeding structure and probably
required to feed. Instead, the successful capture and not to genetic differences. Stramonita haemastoma kept
consumption of P. lapidosa is dependent upon reaching on a diet of P. lapidosa grew significantly longer pro-
the worms deep within their tubes. Phragmatopoma boscises than snails fed oysters, irrespective of where
lapidosa can only escape if it retreats beyond the reach of the snails had originated suggesting that differences in
the snail’s extendable proboscis. Although P. lapidosa proboscis length are inducible. Phenotypic plasticity is
possesses a chitinous operculum that seals the opening common in a number of morphological traits among
of the tube and protects the worm from environmental gastropods. Variations in shell morphology can be in-
stress (Kirtley 1968), it is not adequate protection duced by the presence of predators (Hughes and Elner
against the probing proboscis and scraping radula of S. 1979) and climatic differences (Vermeij 1978; Trussell
haemastoma. 2000). Shell shape and height, and size of the foot vary
On sabellariid reefs, a long proboscis is the most with wave energy (Trussell 1997), and radular teeth of
important feeding structure of S. haemastoma. The some snails can vary in shape depending on prey
proboscis serves the same function on the worm reef as it (Padilla 1998; Reid and Mak 1999). Phenotypic plas-
does in oyster beds; by extending the reach of the mouth, ticity is particularly advantageous for species with
the proboscis allows the snail to feed on items that it dispersive larvae that may settle in environments with a
cannot approach because of its bulky shell. When wide range of conditions. For S. haemastoma, flexibil-
feeding on bivalves, the proboscis reaches well-protected ity in proboscis morphology permits the snail to
soft tissue inside the valves of prey (Carriker and Van broaden its diet and survive in a habitat where its
Zandt 1972; Gunter 1979). We also observed that, when typical food is absent.
feeding in groups, a long proboscis allows several snails Snails from WR are probably genetically similar to
to feed simultaneously on a single gaping oyster. With- those found at ML because larval S. haemastoma spend
out a long proboscis, S. haemastoma would be incapable several months in the plankton (Scheltema 1971;
of capturing P. lapidosa and thus unlikely to establish Dobberdeen and Pechenik 1987), a trait that promotes
populations on sabellariid reefs. genetic exchange and reduces the likelihood of locally
Stramonita haemastoma collected from sabellariid specialized, genetically distinct populations (Janson
reefs had proboscises nearly twice the relative length of 1987). In fact, population dynamics observations at WR
snails from Marineland that feed on bivalves (3.74 and at other sabellariid reef sites suggest that snails on
compared to 1.96 times shell height). A longer proboscis sabellariid reefs disappear (probably perish) before
greatly extends the reach of S. haemastoma and facili- reproducing (Watanabe 2002). Thus, a new population
tates feeding on tubeworms. A short proboscis in this of S. haemastoma is established each year from larvae
environment would make the capture of prey more dif- produced elsewhere, probably from shell-boring popu-
ficult or impossible. Most proboscises of worm-fed lations. Populations on sabellariid reefs appear to be
snails were >70 mm long (many were >100 mm) sug- genetic sinks for other populations, though genetic
gesting that P. lapidosa must retreat at least 70 mm to analysis is required to confirm this.
1028
The energetic cost of foraging on sabellariid reefs is larger sizes while feeding on C. virginica or other bival-
quite different than the cost of foraging on bivalves in ves than non-boring P. lapidosa consumers (Watanabe
other habitats. Time and energy, two related compo- 2002). Nutrition may play an even larger role than time
nents of foraging models, are used to determine the and energy on the overall growth and fitness of S. ha-
value of prey (Hughes 1980). Stramonita haemastoma emastoma.
save a tremendous amount of time feeding on tube- A diet of P. lapidosa may be advantageous for a
worms, consuming worms in a fraction of the time number of other reasons. Because feeding on tubeworms
(<1 h) it takes to eat bivalves (1–3 days). Bivalve prey takes less time, snails may quickly feed and then retreat
are larger than tubeworms and S. haemastoma feeding to shelter. Boring requires snails to remain in place for
on bivalves may fast for several days between meals long periods of time. In the intertidal zone, boring snails
(Gunter 1979). In contrast, S. haemastoma on sabellariid often must endure exposure over multiple tidal cycles
reefs eat less tissue per meal while feeding more fre- and drastic changes in the environment over the course
quently. Laboratory feeding rates of S. haemastoma of a single meal (Menge 1974). Extended bouts of dril-
were between 1.5 and 1.7 worms snailÀ1 dayÀ1 and snails ling render snails vulnerable to desiccation or thermal
thus spent <2 h dayÀ1 feeding. Boggs et al. (1994) stress (Menge 1978a, b). In the intertidal and subtidal
zones, disturbance by waves (Menge 1974; Burrows and
found that when prey was artificially altered to reduce
Hughes 1989; Richardson and Brown 1990) and attack
handling time, boring gastropods increased their feeding
by predators (Richardson and Brown 1992) can result in
rates. Since feeding on worms is fast, snails could
death or the abandonment of a meal with a commen-
potentially increase their daily energy intake. It is
surate loss of many hours of shell drilling. Although
important to note that feeding rates were calculated with
tidal heights and emersion times along the east coast of
snails of only one size class and that feeding rates of S.
Florida are not extreme, sabellariid reefs are exposed to
haemastoma vary with temperature, salinity (Garton and
high temperatures, intense solar radiation, and moderate
Stickle 1980), presence of predators (Richardson and
wave action during tidal exchanges (Watanabe 2002). By
Brown 1992), and wave action (Richardson and Brown
feeding quickly, S. haemastoma avoids most of the
1990). In addition, P. lapidosa shows a seasonal growth
hazards associated with extremely long handling times.
cycle (McCarthy 2001), so differences in energy value per
Stramonita haemastoma survives and feeds on sab-
worm may also influence feeding rates and the amount
ellariid reefs despite the absence of its typical bivalve
of tissue ingested.
prey. Although S. haemastoma possesses feeding struc-
Shell-boring snails expend energy by scraping the
tures specialized for penetrating shells, a phenotypically
surface of a shell with their radula for hours or days. In
plastic proboscis as well as adaptable foraging strategies
addition, the production of enzymes used for the
allow this species to broaden its diet to include tube-
chemical dissolution of shells and wear and tear on the
dwelling polychaetes.
radula (Carriker 1978, 1981) are also costs associated
with boring. Because S. haemastoma on worm reefs do
not drill when feeding on tubeworms, there may be Acknowledgements We would like to thank Drs. J. Lin, R. Tank-
striking differences in the amount of energy required to ersley, and E. Irlandi for their many helpful comments and sug-
feed compared with conspecifics in other habitats. When gestions. We are grateful to Dr. G. Dietl and an anonymous
reviewer whose constructive criticism helped improve and
handling costs are low, prey become more profitable.
strengthen this manuscript. This paper is based on a dissertation
Most bivalves contain more tissue than P. lapidosa, but submitted by J. Watanabe in partial fulfillment of a PhD disserta-
comparisons of the amount of tissue ingested for every tion at Florida Institute of Technology. A Conchologists of America
hour of handling time allows meaningful comparisons of Graduate Fellowship, the Astronaut Trail Shell Club Scholarship,
and an HBOI Summer internship awarded to J. Watanabe, and
food values. Solitary S. haemastoma feeding on solitary
grants from the National Science Foundation awarded to C. Young
mussels (wet mass <2.0 g), clumped oysters (wet mass
provided financial support for the completion of this study.
$35.1 g), and solitary clams (wet mass $63.6 g), in-
gested 0.61, 1.48, and 0.34 mg DW hÀ1, respectively
(Brown and Richardson 1987). Snails feeding on P.
References
lapidosa are much more efficient, ingesting an average of
6.76 mg DW hÀ1 of handling time. Prey such as P. Bayne BL, Newell RC (1983) Physiological energetics of marine
lapidosa that provide relatively more return in a given molluscs. In: Saleuddin ASM, Wilbur KM (eds) The mollusca,
time period are, by definition, more optimal prey vol 4. Physiology Pt 1. Academic, New York, pp 407–515
Boggs CH, Rice JA, Kitchell RA, Kitchell JF (1984) Predation at a
(Hughes 1980). Feeding more efficiently can affect the
snail’s pace: what’s time to a gastropod? Oecologia 62:13–17
snail’s energy budget, and possibly manifest itself as
Brown KM (1997) Size-specific aspects of the foraging ecology of
changes in growth or reproductive output (Bayne and the southern oyster drill Stramonita haemastoma (Kool 1987).
Newell 1983). However, the energy contents of P. lap- J Exp Mar Biol Ecol 214:249–262
idosa and bivalve tissue need to be determined in order Brown KM, Alexander JE (1994) Group foraging in a marine
gastropod predator: benefits and costs to individuals. Mar Ecol
to make more meaningful comparisons. Despite saving
Prog Ser 112:97–105
time and energy, laboratory feeding experiments and Brown KM, Richardson TD (1987) Foraging ecology of the
field population studies have shown that shell-boring S. southern oyster drill Thais haemastoma (Gray): constraints on
haemastoma grow much more rapidly and attain much prey choice. J Exp Mar Biol Ecol 114:123–141
1029
Burrows MT, Hughes RN (1991) Variation in foraging behaviour McCarthy DA (2001) Life-history patterns and the role of distur-
among individuals and populations of dogwhelks, Nucella lapil- bance in intertidal and subtidal populations of the polychaete
lus: natural constraints on energy intake. J Anim Ecol 60:497–514 Phragmatopoma lapidosa lapidosa (Kinsberg 1867) in the
Butler PA (1985) Synoptic review of the literature on the southern tropical Western Atlantic. Dissertation, Kings College
oyster drill Thais haemastoma floridana. NOAA Technical McGraw KA, Gunter G (1972) Observations on killing of the
Report NMFS 35:1–12 Virginia oyster by the gulf oyster borer, Thais haemastoma, with
Carriker MR (1978) The chemical mechanism of shell dissolution evidence for a paralytic secretion. Proc Nat Shellfish Assoc
by predatory boring gastropods: a review and an hypothesis. 62:95–97
Malacalogia 17:143–156 Menge JL (1974) Prey selection and foraging period of the preda-
Carriker MR (1981) Shell penetration and feeding by naticacean ceous rocky intertidal snail, Acanthina punctulata. Oecologia
and muricacean predatory gastropods: a synthesis. Malacologia 17:293–316
20:403–422 Menge BA (1978a) Predation intensity in a rocky intertidal
Carriker MR, Van Zandt D (1972) Predatory behavior of a shell- community: relation between predator foraging activity and
boring muricid gastropod. In: Winn HE, Olla BL (eds) environmental harshness. Oecologia 32:1–16
Behavior of marine animals. Plenum, New York, pp 157–244 Menge BA (1978b) Predation intensity in a rocky intertidal com-
Dobberdeen RA, Pechenik JA (1987) Comparison of larval bio- munity: effect of an algal canopy, wave action and desiccation
energetics of two marine gastropods with widely differing on predator feeding rates. Oecologia 32:17–35
lengths of planktonic life, Thais haemastoma canaliculata and Padilla DK (1998) Inducible phenotypic plasticity of the radula in
Crepidula fornicata. J Exp Mar Biol Ecol 109:173–191 Lacuna (Gastropoda: Littorinidae). Veliger 41:201–204
Garton DW (1986) Effect of prey size on the energy budget of a Reid DG, Mak YM (1999) Indirect evidence for ecophenotypic
predatory gastropod, Thais haemastoma canaliculata. J Exp plasticity in radular dentition of Littoraria species (Gastropoda:
Mar Biol Ecol 98:21–33 Littorinidae). J Moll Stud 65:355–370
Garton D, Stickle WB (1980) Effects of salinity and temperature on Richardson TD, Brown KM (1990) Wave exposure and prey size
the predation rate of Thais haemastoma on Crassostrea virginica selection in an intertidal predator. J Exp Mar Biol Ecol
spat. Biol Bull 158:49–57 142:105–120
Gore RH, Scotto LE, Becker LJ (1978) Community composition, Richardson TD, Brown KM (1992) Predation risk and feeding in
stability, and trophic partitioning in decapod crustaceans an intertidal predatory snail. J Exp Mar Biol Ecol
inhabiting some subtropical sabellariid worm reefs. Bull Mar 163:169–182
Sci 28:221–248 Scheltema RS (1971) Larval dispersal as a means of genetic
Gunter G (1979) Studies of the southern oyster borer, Thais exchange between geographically separated populations of
haemastoma. Gulf Res Rept 6:249–260 shallow-water benthic marine gastropods. Biol Bull
Hughes RN (1980) Optimal foraging theory in the marine context. 140:284–322
Oceanogr Mar Biol Annu Rev 18:423–481 Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol
Hughes RN, Elner RW (1980) Tactics of a predator, Carcinus Syst 2:369–404
maenas, and morphological responses of the prey, Nucella Trussell GC (1997) Phenotypic plasticity in the foot size of an
lapillus. J Anim Ecol 48:65–78 intertidal snail. Ecology 78:1033–1048
Ingham RE, Zishke JA (1977) Prey preferences of carnivorous Trussell GC (2000) Phenotypic clines, plasticity, and morphological
intertidal snails in the Florida Keys. Veliger 20:49–51 trade-offs in an intertidal snail. Evolution 54:151–166
Janson K (1987) Allozyme and shell variation in two marine snails Vermeij GJ (1978) Biogeography and adaptation: patterns of
(Littorina, Prosobranchia) with different dispersal abilities. Biol marine life. Harvard University Press, Cambridge
J Linn Soc 30:245–256 Watanabe JT (2002) The ecology of the southern oyster drill,
Kirtley DW (1968) The reef builders. Nat Hist (NY) 77:40–45 Stramonita haemastoma (Gastropoda: Muricidae) on Florida
Liu LL, Foltz DW, Stickle WB (1991) Genetic population structure sabellariid worm reefs. Dissertation, Florida Institute of Tech-
of the southern oyster drill Stramonita (=Thais) haemastoma. nology, Melbourne
Mar Biol 111:71–79
DOI 10.1007/s00227-005-0152-9
R ES E AR C H A RT I C L E
Jeffrey T. Watanabe Æ Craig M. Young
Feeding habits and phenotypic changes in proboscis length
in the southern oyster drill, Stramonita haemastoma
(Gastropoda: Muricidae), on Florida sabellariid worm reefs
Received: 2 May 2005 / Accepted: 22 September 2005 / Published online: 15 November 2005
Ó Springer-Verlag 2005
attacks and consumes worms in 15–50 min. In the lab-
Abstract The southern oyster drill, Stramonita (= Thais,
oratory, oyster drills consumed 1.7 worms per day,
Kool 1987) haemastoma, is a common intertidal and
spending <1 h each day feeding. On sabellariid reefs,
subtidal predator in the southeastern United States. It
differences in feeding, handling costs, and prey value, are
uses specialized feeding structures and foraging strate-
likely to have a significant effect on the ecology and life
gies to bore holes through the shell of its bivalve prey.
history of S. haemastoma in this habitat.
However, on the east coast of Florida, S. haemastoma, is
common on sabellariid worm reefs constructed by the
polychaete Phragmatopoma lapidosa (Walton Rocks
Beach, Florida, 27°17¢N, 80°12¢W), a habitat where the
snail’s typical prey are scarce. From 1999 to 2001, we Introduction
examined the feeding habits of S. haemastoma on sab-
ellariid reefs and the behavioral and morphological Many predators exhibit specialized foraging strategies
responses of S. haemastoma that accompanied switching and morphological adaptations that have arisen in re-
from a diet of bivalves to sabellariids. On worm reefs sponse to selective pressures imposed by specific types of
S. haemastoma feeds on P. lapidosa by inserting the prey (Schoener 1971). Shell-boring in gastropods is a
proboscis deep into a worm’s tube. Worm-feeding snails feeding strategy that permits some snails to feed on
had longer proboscises ($3.7 times shell height) than bivalves and other shelled benthic invertebrates— prey
bivalve-feeding conspecifics ($2.0 times shell height). whose defenses present significant challenges to attack-
Snails raised on different diets showed significant dif- ers. To circumvent these defenses, shell-boring gastro-
ferences in proboscis length suggesting that the pro- pods drill a hole through the calcareous shell of their
boscis length is phenotypically plastic. Whereas typical prey using a combination of radular scraping and
oyster drills must bore holes for days before ingesting chemical dissolution. An accessory boring organ secretes
prey, S. haemastoma on worm reefs avoids boring and enzymes intermittently, which helps soften and dissolve
the area being drilled (Carriker 1978, 1981). After a hole
is made in the shell, a long proboscis extends into the
Communicated by J.P.Grassle, New Brunswick shell and the soft tissue is torn off and ingested. Thus,
the ability to bore through shell and then feed on its
J. T. Watanabe
contents required the evolution of several anatomical,
Harbor Branch Oceanographic Institution,
5600 US 1 North, Ft, Pierce, FL 34946, USA physiological, and behavioral innovations.
Feeding on an individual shelled prey item may take
C. M. Young
several hours to several days, requiring a substantial
Florida Institute of Technology, Melbourne,
commitment of both time and energy. The significant
150 W. University Blvd, Melbourne, FL 32901, USA
handling costs associated with shelled prey have led to
Present address: J. T. Watanabe (&) the evolution of foraging strategies that reduce handling
Department of Biology, Ohlone College,
time and other costs, and maximize energy intake
Fremont, CA 94539, USA
(Hughes 1980). When given a choice, shell-boring snails
E-mail: jwatanabe@ohlone.edu
tend to select prey of optimal size and will choose more
Tel.: +1-510-6596000
Fax: +1-510-6596244 easily accessible or energetically rich species of prey over
others (Garton 1986; Brown and Richardson 1987;
C. M. Young
Brown 1997). Feeding behaviors such as attacking the
Oregon Institute of Marine Biology,
margin or lip of shells where defenses are weakest
Charleston, OR 97420, USA
1022
canaliculata-like are more common along the Gulf coast
(Gunter 1979), or foraging in groups (Brown and Alex-
of Louisiana, Mississippi, and Florida, while floridana-
ander 1994) save time and energy. Some larger oyster
like snails are more prevalent in Texas and at two sites
drills may avoid boring altogether by secreting a toxin
on the Atlantic coast of Florida. However, the same
that causes bivalves to gape (McGraw and Gunter 1972).
study found that genetic differences did not correlate
Given the specialized nature of their feeding struc-
with differences in shell or radular morphology, char-
tures and foraging habits, shell-boring gastropods often
acteristics previously used to differentiate the subspecies.
occur where bivalves and other shelled prey are abun-
In this study, we collected bivalve-feeding S. haemas-
dant. In the southeastern United States, the southern
toma from a site on the Atlantic coast of Florida where
oyster drill, Stramonita haemastoma, feeds on the eastern
Liu et al. (1991) found 114/128 floridana-like snails, 7/
oyster, Crassostrea virginica (reviewed by Butler 1985),
128 canaliculata-like, and 7/128 possible hybrids.
mussels, Ischadium recurvum, and clams Rangia cuneata
Unfortunately, no genetic analyses have been conducted
(Brown and Richardson 1987). In the Florida Keys, they
on sabellariid reef populations of S. haemastoma where
feed on two species of tree oysters, Isognomon bicolor
our other snails were collected. In the absence of any
and I. radiatus, the mussel Brachidontes exustus, and the
information to the contrary, we assume that snails from
barnacle Tetraclita squamosa (Ingham and Zishke 1977).
both our study sites belong to the subspecies floridana.
They also attack the bivalves Donax variabilis, Perna
Other than allozyme differences revealed by Liu et al.
perna, Anomia simplex, Mercenaria mercenaria, and the
(1991), no significant biological differences between the
gastropod Crepidula plana and cannibalize smaller con-
subspecies have been established.
specifics (Butler 1985).
However, on the Atlantic coast of Florida, popula-
tions of S. haemastoma occur on sabellariid worm reefs,
Materials and methods
a habitat where large populations of bivalve prey are
unavailable to them. Sabellariid reefs are formed by
Study sites
large aggregations of the tube-building polychaete
Phragmatopoma lapidosa (Sabellariidae). Huge intertidal
Stramonita (= Thais, Kool 1987) haemastoma were
and subtidal mounds consisting of thousands of sand
collected from two sites on the east coast of Florida,
tubes form reefs, and each mound may cover several
USA, between 1999 and 2001. Walton Rocks Beach
square meters (Kirtley 1968). We witnessed S. haemas-
(27°17¢N, 80°12¢W) (WR) is located on the ocean side of
toma living directly on the worm mounds and sheltering
a barrier island, approximately 65 km north of Palm
in the cracks and crevices of the reef when not feeding.
Beach, Florida. A sandy beach slopes into the sea where
On sabellariid reefs, oyster drills feed primarily on P.
scattered limestone coquina foundations support
lapidosa. For a predator that specializes on bivalves,
mounds of intertidal and subtidal P. lapidosa worm reef.
switching to a diet of tubeworms is a major shift in
Snails <25 mm in shell height were collected at low tide
foraging strategy. Differences in prey defense also pres-
primarily between the months of November and Feb-
ent challenges that must be overcome for S. haemastoma
ruary. Clumps of worm tubes were collected regularly to
to survive on sabellariid reefs.
feed the snails and for use in experiments. Both worms
Stramonita haemastoma is considered a pest of the
and snails were transported in buckets of seawater to
commercial oyster industry and as a result, its feeding
our laboratory at Harbor Branch Oceanographic Insti-
habits on oysters and on other bivalves have been
tution (HBOI) where they were maintained in aquaria at
extensively studied (review by Butler 1985). However, no
room temperature ($23°C).
information exists on the feeding habits of S. haemas-
Stramonita haemastoma from WR were compared
toma on P. lapidosa worm reefs. We examined feeding
with snails at Marineland, Florida (29°40¢N, 81°12¢W)
behavior, feeding rate, and handling time of S. ha-
(ML), approximately 270 km further north. At this site,
emastoma feeding on P. lapidosa tubeworms. The long
snails occur on intertidal limestone boulders that form
proboscis of S. haemastoma is its most functionally
groins perpendicular to the beach. Wave action and sand
important feeding structure on worm reefs, so we com-
surrounding the boulders probably prevents emigration
pared the proboscises of worm predators with those of
from the study site. P. lapidosa does not occur at this site
bivalve predators from another habitat to see if differ-
and snails were found feeding on the small ($7 mm)
ences in habitat and prey were correlated with proboscis
bivalve Lyonsia hyalina and the barnacle Balanus
length. Finally, snails from different habitats were
amphitrite which occurs slightly higher in the intertidal.
maintained on diets of worms or bivalves to determine if
Snails of shell height 20–35 mm were collected at low tide
changes in proboscis length are inducible.
and transported in buckets of seawater to the laboratory.
In the southeast United States, two subspecies, S.
We measured shells with vernier calipers to the nearest
haemastoma canaliculata (Gray 1839) and S. haemas-
0.1 mm from the siphon to the tip of the spire. Prior to
toma floridana (Conrad 1837) have been described based
the experiments, WR snails were maintained on a diet of
on differences in shell and radular morphology. A
P. lapidosa. Because the bivalve Lyonsia hyalina, was not
population genetics study of snails in this region iden-
readily available near the laboratory, ML snails were fed
tified two genetically differentiated groups of S. ha-
the oyster C. virginica, collected from a nearby seawall.
emastoma (Liu et al. 1991). Snails characterized as
1023
60
50
Time (min)
40
30
20
10
24 26 28 30 32 34 36 38 40
Shell Height (mm)
Fig. 2 Stramonita haemastoma. Relationship between shell height
and time to consume a single P. lapidosa in a synthetic tube (n =
12, y = 0.938x + 63.575, r2 = 0.208)
Fig. 1 Stramonita haemastoma. Attack on Phragmatopoma lapid-
pipettes (Fig. 1b). Six tubes (interior diameter 3 mm)
osa in a A sand tube constructed by P. lapidosa on plexiglass. b A
were mounted and glued in a frame of two 15·20 cm2
1-ml plastic pipette (Photo W. Tyler). Time-lapse video and lines on
acrylic sheets. The sheets had holes to hold the tubes
pipette were used to measure length of snail proboscis. Arrow
indicates tip of snail’s proboscis. Scale bar 10 mm in place, which were spaced two per row, with open-
ings mounted flush with one sheet. Six tubes were used
to increase the likelihood that a snail would encounter
Feeding behavior, handling time, and proboscis length
a worm. Individual worms were removed from their
sand tubes and placed inside the pipettes, posterior
Stramonita haemastoma attack and consume P. lapidosa
end first, with the head towards the opening of the
within the worm tubes, making it difficult to observe
pipette. Three or four snails at a time were labeled
feeding. We, therefore, developed two new methods to
with nail polish and introduced to a 15-l seawater
observe the feeding behavior of S. haemastoma on P.
aquarium containing the pipettes and worms. Using a
lapidosa. Individual tubeworms were cultured on trans-
Panasonic time-lapse video recorder, we videotaped
parent acrylic sheets and encouraged to build natural
the aquarium for 72 h to observe feeding behavior
sand tubes on the transparent surface (Fig. 1a). A sim-
over extended periods of time. As snails fed, they
ilar technique was previously used to observe the
extended their proboscis down the tube, and the
behavior of P. lapidosa within sand tubes (J. Pawlik,
worms either retreated or were pushed by the pro-
personal communication). We broke apart clumps of
boscis. As the worms retreated, S. haemastoma,
worm reef and isolated individual P. lapidosa within
their sand tubes. Each tube was shortened to $15 mm, extended its proboscis further. Markings on the tube
visible in the video replay enabled measurement of
making the tubes approximately the same size as the
worms, and placed them on 10·10 cm2 clear acrylic proboscis length. Whenever possible, handling time
(the time from initial proboscis extension until the
sheets in an aerated seawater aquarium. The remaining
worm was consumed) was recorded from video foot-
tube fragments were crushed into individual sand grains.
age or real-time observations. The aquarium was near
A trail of sand was placed in front of each worm tube.
a window and so natural light and dark cycles existed
When left undisturbed for 2–3 weeks, the worms
during the duration of the experiment.
reconstructed tubes on the acrylic sheet. This created an
We compared the proboscis lengths of snails from the
‘ant farm’ effect that allowed a view of the worm within
WR and ML sites to determine if different types of
the tube. During tube building, worms were fed the
available prey (and the different methods of handling
diatom Chaetoceros gracilis. Stramonita haemastoma
these prey) were related to proboscis length. After each
was then placed with the worm and the sheet was in-
proboscis was measured, we removed the snail from the
verted under water. Under a dissecting microscope,
aquarium and measured shell height. Shell height to
feeding behavior was observed from above with the
proboscis length regressions were compared between
worm and snail on the opposite side of the clear sheet.
the two sites, using ANCOVA, with shell height as a
Snail feeding behavior was also observed in artifi-
covariate to eliminate the effects of snail size.
cial tubes made from 1-ml clear graduated plastic
1024
Phenotypic plasticity determine the number consumed by the snail. Feeding
rate (worms per day) was calculated as the number of
Stramonita haemastoma feeding on worms had much worms consumed during the experiment, divided by
longer proboscises than snails feeding on oysters. To days of the study.
determine if proboscis length changes phenotypically
with a change in diet, we maintained separate groups of
Phragmatopoma lapidosa tissue dry-mass
snails from WR and ML on diets of either C. virginica
($65 mm from hinge to posterior shell edge) or P. lap-
To determine the amount of tissue consumed by the
idosa. At the beginning of the experiment, snails from
snails, we calculated the average dry tissue weight of
WR were slightly smaller (22.8±2.4 mm) than those
individual P. lapidosa collected at WR in April 2001.
from ML (26.3±3.2 mm). Snails of this size range have
One hundred worms were removed from their tubes and
not yet attained reproductive maturity and were re-
fixed in 10% formalin and sea water. Body length of
cruited within 6 months of collection (unpublished).
each worm was measured to the nearest 0.01 mm from a
Stramonita haemastoma may attain shell heights of
digital photograph, using University of Texas Health
>100 mm and live for several years and have been
Science Center San Antonio (UTHSCS1A) imaging
known to grow 25 mm in just 30 days in the laboratory
program version 2.0. Undamaged worms (n=41) were
(Butler 1987).
then oven-dried at 60°C for 24 h and weighed on a
Snails were maintained in five, 47-l aquaria, each di-
vided into 12, 12 · 6 · 14 cm3 chambers. Snails were Mettler AE 163 analytical balance. After total body
weight was measured, the operculum was removed from
paired within chambers because the experiment also
the worm and weighed to determine the percentage of
measured reproductive output (Watanabe 2002). Each
worm mass attributable to the operculum, the only part
tank had six snails from each habitat fed with each type
of the worm that is not consumed by the snail.
of prey. Each chamber received either one clump of
The dry tissue consumed per day was calculated by
Phragmatopoma lapidosa (>200 individuals) every
multiplying the number of worms eaten per day from the
4 weeks, or one cracked C. virginica oyster every 10–
feeding experiment by the average dry tissue weight
14 days. Oysters were cracked open with a hammer so
without the operculum. P. lapidosa spawns when stres-
that regular feeding intervals could be maintained and
sed, and dry mass did not account for missing mass due
feeding would not be delayed by individual differences in
to release of eggs or sperm when worms were originally
the timing of shell-boring. This method should not affect
removed from their tubes. When P. lapidosa are being
the way the proboscis is extended when feeding on
consumed by S. haemastoma, the worms may likely
oysters. A preliminary study showed no significant dif-
spawn before being eaten, and snails may not recover
ference in growth of snails that fed on opened or closed
that biomass anyway. This was not, however, observed
oysters (Watanabe 2002).
in our feeding experiments because worms released their
After 11 months, snails were removed from aquaria
gametes during the experimental setup prior to the
and proboscises were measured as described previously.
introduction of the snails. Phragmatopoma lapidosa are
Fifteen snails from each of the four site-prey combina-
capable of spawning the year round (McCarthy 2001),
tions were measured. Proboscis lengths were compared
but at WR settlement was heaviest in September and
using a two-way factorial ANCOVA with prey (fixed)
October and abundance declined by August (Watanabe
and site (random) as the factors and shell height as the
2002).
covariate.
Profitability of prey, (Brown and Richardson 1987),
was calculated as the amount of dry tissue consumed per
hour of feeding effort. The mean dry mass of P. lapidosa
Feeding rate
(without the operculum) was divided by the mean time it
took snails to consume a single worm (as determined by
We estimated feeding rate of S. haemastoma on P. lap-
the handling time studies). This yielded the amount of
idosa in an experiment in April 2001. We put S. ha-
dry tissue consumed per hour of handling time.
emastoma (mean shell height 23.3±0.8 mm) in 11
replicate, 2-l plastic containers of aerated seawater with
clumps of worm reef (11–15 worms clumpÀ1) for 7 days.
Results
Three 2-l containers holding only worm clumps were
used as controls. Prior to the experiment, all snails were
Feeding behavior and handling time
kept in tanks with an ample supply of P. lapidosa
clumps. After 7 days, the remaining worms were coun-
After S. haemastoma were placed in tanks containing P.
ted to determine the number of worms consumed. Half
lapidosa, the snails either searched for prey, or became
the water in each container was replaced twice during
inactive and did not move for some time. Videotaped
the experiment and all containers were kept at room
observations over 72 h showed an apparently random
temperature ($23 C). After 7 days, worm clumps were
activity pattern that did not correlate with any diurnal
broken apart and the number of worms remaining in
or tidal patterns.
each replicate was subtracted from the initial number to
1025
Like other predatory gastropods, S. haemastoma 180
made lateral movements of the siphon while searching 160
for prey, presumably testing the water from different
Proboscis Length (mm)
140
directions. Snails found the opening of the worm tubes
120
with their siphons, often touching the tentacles of
P. lapidosa in the process. The worms retracted upon 100
contact but generally did not retreat down their tubes 80
immediately. Snails initiated feeding by covering the 60
external opening of the worm tube with the anterior
40
portion of the foot. The snails then inserted their Walton Rocks
20
proboscises into the opening of the tube. When the Marineland
proboscises touched the tentacles or chitinous opercu- 0
lum of P. lapidosa, the worms retreated into the tube. 22 24 26 28 30 32 34 36 38 40 42 44
Shell Height (mm)
The snails followed the worms with their proboscises,
rasping with their radula in an apparent attempt to
Fig. 3 Stramonita haemastoma. Relationship between shell height
slow down or capture the retreating worm. P. lapidosa and proboscis length for snails from two populations with different
was captured when it could not retreat any deeper, or prey (n = 19 for each). Shell height was not a good predictor of
proboscis length for snails from WR (y = 0.458x + 106.795, r2 =
when the radula of S. haemastoma caught the opercular
0.010) nor snails from ML (y = 1.839x + 3.695, r2 = 0.477).
plate of the worm. The operculum was slightly smaller
Proboscises of snails preying on P. lapidosa predators from WR
than the diameter of the tube and allowed movement were significantly longer than bivalve predators from ML (Table 1)
of the worm up or down the tube while keeping the
head of the worm covered. S. haemastoma scraped at
the operculum until it tilted to one side, rendering the
Proboscis length
soft head of P. lapidosa vulnerable to attack. Once the
soft tissue was accessed, S. haemastoma tore bits of
Stramonita haemastoma from WR that fed on P.
flesh from its prey. In the tube, some snails slowly
lapidosa had much longer proboscises than conspecifics
retracted the proboscis as they fed, pulling the worm
from ML that fed on bivalves (Fig. 3, Table 1).
toward the opening of the tube. Near the tip of the
Differences in proboscis length varied with habitat
proboscis, microscopic particles of detritus and sand
and were not explained by differences in shell height.
moved rhythmically back and forth as the snail fed,
Individuals from WR 26.1 to 42.5 mm shell height had
suggesting a sucking or pumping force during feeding.
proboscises 85.1–159.6 mm long. Proboscis length was
When feeding on bivalves, the muscular proboscis
not significantly correlated with shell size; probos-
pumps liquefied oyster tissue from the shell of prey.
cises ranged from 2.34 to 5.46 times the height of the
In addition to bringing particles to the mouth, the
suction helped S. haemastoma slow down the retreat of
P. lapidosa and pulled the worm toward the proboscis.
S. haemastoma used two different methods of ingesting Table 1 Stramonita haemastoma ANCOVA table comparing the
effect of habitat on proboscis lengths with shell height as the co-
the remainder of the prey. In some cases, snails con-
variate
sumed the worms with the proboscis extended into the
tubes; in other cases, they pulled the worms to the Source of df SS MS F P
opening of the tube before ingestion. Tiny pieces of variation
tissue moved in rhythmic pulses down the length of the
Shell 1 984.46 984.46 3.01 0.091
semi-transparent proboscis. S. haemastoma ate all soft
Site 1 31,443.95 31,443.95 96.27 <0.001
parts of the polychaete but never consumed the chi- Error 35 11,431.33 326.61
tinous operculum. Total 37 47,533.87
Stramonita haemastoma rapidly attacked and con-
sumed individual P. lapidosa when compared to other
types of prey. Feeding times on P. lapidosa ranged Table 2 Stramonita haemastoma ANCOVA table comparing the
from 14 to 50 min. In 13 timed attacks in artificial tubes, effect of habitat and diet on proboscis lengths of snails with shell
S. haemastoma consumed P. lapidosa in a mean time of height as the covariate for groups of snails in the laboratory
32.2±8.3 (SD, range 14–50) min. In another study,
Source of df SS MS F P
similarly sized S. haemastoma took 20 h to feed on the
variation
mussel I. recurvum, and up to 70 h to consume clumped
C. virginica (Brown and Richardson 1987). Snails fed Shell 1 648.51 648.51 2.20 0.144
continuously once they began ingesting the tissue and Site 1 6.15 6.15 0.02 0.886
Prey 1 3,049.74 3,049.74 10.33 < 0.01
stopped only after all soft tissue was eaten. The size of
Site · Prey 1 913.35 913.35 3.09 0.085
snails did not show a strong relationship with feeding
Error 55 16,237.43 295.23
time (Fig. 2). Profitability for snails feeding on worms Total 59 20,291.90
was 6.76 mg DW hÀ1 of handling time.
1026
140
P. lapidosa diet
Proboscis length / Shell height
Walton Rocks C. virginica diet
4
120
100 3
80
2
Proboscis Length (mm)
60
P. lapidosa
1
C. virginica
40
20 25 30 35 40 45 50 55 0
Marineland
Walton Rocks
140 Site
Marineland
120 Fig. 5 Stramonita haemastoma. Ratio of proboscis length to shell
height for snails from two different sites (WR and ML) maintained
for 9 months on diets of P. lapidosa or C. virginica. Error bars = 1
100
SD (n = 16 for each site-prey combination)
80
2.02±0.34 times shell height (Fig. 5). On a diet of
60
Phragmatopoma lapidosa, snails from ML had probos-
cises 3.21±0.76 times the height of the shell, whereas
40
snails from the same site fed oysters, had proboscises
20 25 30 35 40 45 50 55
only 1.97±0.38 times the shell height. By the end of the
Shell Height (mm) experiment, nearly all snails raised on oysters had larger
shells than snails fed P. lapidosa, irrespective of where
Fig. 4 Stramonita haemastoma. Relationship between shell height
the snails had originated.
and proboscis length from two different sites (WR and ML)
maintained for 9 months on diets of P. lapidosa or Crassostrea
virginica. Proboscises of snails fed P. lapidosa were proportionally
longer than those fed C. virginica (Table 2). Regressions indicate
Phragmatopoma lapidosa length and mass
that shell height was not a good predictor of proboscis length for
snails from WR maintained on P. lapidosa (y = 0.171x + 85.884,
r2 = 0.003) or on C. virginica (y = 0.336x + 99.745, r2 = 0.025) Phragmatopoma lapidosa collected in April 2001 had a
nor for snails from ML maintained on P. lapidosa (y = 0.387x + mean length of 14.55±2.92 mm (range 8.34–20.94) and
84.660, r2 = 0.01) or on C. virginica (y = 1.671x + 11.492, r2 = a dry mass of 4.233±1.584 mg mmÀ1 wormÀ1 (n = 41)
0.376)
(range 1.2–8.8 mg mmÀ1 wormÀ1). The average amount
of consumable tissue (without the operculum) was
snail’s shell (mean 3.74±0.85 SD). One individual 3.664±1.419 mg. The operculum of P. lapidosa made up
with a 28.7 mm shell had a proboscis 156.6 mm long.
Snails from ML 24.5 to 39.4 mm shell height had
proboscises 42.6–79.0 mm long. Proboscises ranged
from 1.44 to 2.67 times the height of their shells, with a 1.0 y = 1.368x -1.0489 r2 = 0.488
mean of 1.96±0.30 (SD) times shell height. Thus, snails
from WR that normally feed on worms can extend their 0.8
Log Weight (mg)
proboscises about 1.9 times further than snails from ML
that normally feed on bivalves. 0.6
Stramonita haemastoma maintained in the laboratory
for 11 months on a diet of P. lapidosa had significantly 0.4
longer proboscises than snails fed oysters irrespective of
0.2
size or original habitat (Fig. 4, Table 2). Regressions
indicate that shell height was not a good predictor of
0.0
proboscis length for snails from WR maintained on
P. lapidosa (y = 0.171x+85.884, r2 = 0.003) or on
C. virginica (y = 0.336x+99.745, r2 = 0.025), nor for 0.8 0.9 1.0 1.1 1.2 1.3 1.4
snails from ML maintained on P. lapidosa (y = 0.387x+ Log Length (mm)
84.660, r2 = 0.01) or on C. virginica (y = 1.671x+
11.492, r2 = 0.376). Fig. 6 Phragmatopoma lapidosa. Relationship between length and
dry mass of worms from WR in April 2001 (n = 41) All values were
Snails from WR fed tubeworms had proboscises log transformed and mass increased significantly with length.
2.62±0.73 times shell height, whereas snails from the Worm length increased with mass (y = 1.368x À1.0489, r2 =
same site fed C. virginica had shorter proboscises, 0.488)
1027
escape an attack. Using grains of sand, P. lapidosa
approximately 13.6±3.6% of the total dry mass of the
increases the length and diameter of its tube as it
worm. Dry mass of P. lapidosa was positively related to
matures. The most recently constructed part of the tube
worm length (Fig. 6).
is near the opening and is wider than older parts of the
tube which are built when the worm is smaller. Even
though sabellariid reefs may be >1 m tall, the length of
Feeding rate
tube occupied by the worm is much shorter, leaving
worms within reach of S. haemastoma. Worms could
Stramonita haemastoma consumed a total of 10.8±2.7
potentially respond to predation pressure by building
(SD) Phragmaopoma lapidosa in 7 days. Snails ate about
longer tubes, but this would create larger worm mounds
5 to 14 worms during the feeding period. Their mean
daily feeding rate was 1.57±0.38 worms snailÀ1 dayÀ1, that are less stable and more likely to break under wave
equivalent to 5.76±1.40 mg DW snailÀ1 dayÀ1. All pressure. Also, longer tubes in the intertidal might reach
above the water line and would increase exposure and
control worms remained alive during the duration of the
stress during low tide.
experiment. One snail that escaped from its tank and
At WR two non-shell-boring gastropods, Pollia tincta
died was not included in the measurements.
(Buccinidae) and Leucozonia nassa (Fasciolaridae), were
observed feeding on P. lapidosa with long proboscises
Discussion inserted in worm tubes, though these species were rare
compared to S. haemastoma. Decapod crustaceans
The feeding habits of S. haemastoma living on sabellariid (Gore et al. 1978) and S. haemastoma probably account
worm reefs differ from conspecifics in more typical for the greatest predation pressure on P. lapidosa where
habitats. Major differences in handling costs, prey de- they co-occur.
fense, and mode of feeding affect foraging on the reefs. Differences in proboscis length between snails
A diet of worms does not require snails to bore through collected from WR and ML are attributable to phe-
shell, drastically reducing the amount of time and energy notypic plasticity of the feeding structure and probably
required to feed. Instead, the successful capture and not to genetic differences. Stramonita haemastoma kept
consumption of P. lapidosa is dependent upon reaching on a diet of P. lapidosa grew significantly longer pro-
the worms deep within their tubes. Phragmatopoma boscises than snails fed oysters, irrespective of where
lapidosa can only escape if it retreats beyond the reach of the snails had originated suggesting that differences in
the snail’s extendable proboscis. Although P. lapidosa proboscis length are inducible. Phenotypic plasticity is
possesses a chitinous operculum that seals the opening common in a number of morphological traits among
of the tube and protects the worm from environmental gastropods. Variations in shell morphology can be in-
stress (Kirtley 1968), it is not adequate protection duced by the presence of predators (Hughes and Elner
against the probing proboscis and scraping radula of S. 1979) and climatic differences (Vermeij 1978; Trussell
haemastoma. 2000). Shell shape and height, and size of the foot vary
On sabellariid reefs, a long proboscis is the most with wave energy (Trussell 1997), and radular teeth of
important feeding structure of S. haemastoma. The some snails can vary in shape depending on prey
proboscis serves the same function on the worm reef as it (Padilla 1998; Reid and Mak 1999). Phenotypic plas-
does in oyster beds; by extending the reach of the mouth, ticity is particularly advantageous for species with
the proboscis allows the snail to feed on items that it dispersive larvae that may settle in environments with a
cannot approach because of its bulky shell. When wide range of conditions. For S. haemastoma, flexibil-
feeding on bivalves, the proboscis reaches well-protected ity in proboscis morphology permits the snail to
soft tissue inside the valves of prey (Carriker and Van broaden its diet and survive in a habitat where its
Zandt 1972; Gunter 1979). We also observed that, when typical food is absent.
feeding in groups, a long proboscis allows several snails Snails from WR are probably genetically similar to
to feed simultaneously on a single gaping oyster. With- those found at ML because larval S. haemastoma spend
out a long proboscis, S. haemastoma would be incapable several months in the plankton (Scheltema 1971;
of capturing P. lapidosa and thus unlikely to establish Dobberdeen and Pechenik 1987), a trait that promotes
populations on sabellariid reefs. genetic exchange and reduces the likelihood of locally
Stramonita haemastoma collected from sabellariid specialized, genetically distinct populations (Janson
reefs had proboscises nearly twice the relative length of 1987). In fact, population dynamics observations at WR
snails from Marineland that feed on bivalves (3.74 and at other sabellariid reef sites suggest that snails on
compared to 1.96 times shell height). A longer proboscis sabellariid reefs disappear (probably perish) before
greatly extends the reach of S. haemastoma and facili- reproducing (Watanabe 2002). Thus, a new population
tates feeding on tubeworms. A short proboscis in this of S. haemastoma is established each year from larvae
environment would make the capture of prey more dif- produced elsewhere, probably from shell-boring popu-
ficult or impossible. Most proboscises of worm-fed lations. Populations on sabellariid reefs appear to be
snails were >70 mm long (many were >100 mm) sug- genetic sinks for other populations, though genetic
gesting that P. lapidosa must retreat at least 70 mm to analysis is required to confirm this.
1028
The energetic cost of foraging on sabellariid reefs is larger sizes while feeding on C. virginica or other bival-
quite different than the cost of foraging on bivalves in ves than non-boring P. lapidosa consumers (Watanabe
other habitats. Time and energy, two related compo- 2002). Nutrition may play an even larger role than time
nents of foraging models, are used to determine the and energy on the overall growth and fitness of S. ha-
value of prey (Hughes 1980). Stramonita haemastoma emastoma.
save a tremendous amount of time feeding on tube- A diet of P. lapidosa may be advantageous for a
worms, consuming worms in a fraction of the time number of other reasons. Because feeding on tubeworms
(<1 h) it takes to eat bivalves (1–3 days). Bivalve prey takes less time, snails may quickly feed and then retreat
are larger than tubeworms and S. haemastoma feeding to shelter. Boring requires snails to remain in place for
on bivalves may fast for several days between meals long periods of time. In the intertidal zone, boring snails
(Gunter 1979). In contrast, S. haemastoma on sabellariid often must endure exposure over multiple tidal cycles
reefs eat less tissue per meal while feeding more fre- and drastic changes in the environment over the course
quently. Laboratory feeding rates of S. haemastoma of a single meal (Menge 1974). Extended bouts of dril-
were between 1.5 and 1.7 worms snailÀ1 dayÀ1 and snails ling render snails vulnerable to desiccation or thermal
thus spent <2 h dayÀ1 feeding. Boggs et al. (1994) stress (Menge 1978a, b). In the intertidal and subtidal
zones, disturbance by waves (Menge 1974; Burrows and
found that when prey was artificially altered to reduce
Hughes 1989; Richardson and Brown 1990) and attack
handling time, boring gastropods increased their feeding
by predators (Richardson and Brown 1992) can result in
rates. Since feeding on worms is fast, snails could
death or the abandonment of a meal with a commen-
potentially increase their daily energy intake. It is
surate loss of many hours of shell drilling. Although
important to note that feeding rates were calculated with
tidal heights and emersion times along the east coast of
snails of only one size class and that feeding rates of S.
Florida are not extreme, sabellariid reefs are exposed to
haemastoma vary with temperature, salinity (Garton and
high temperatures, intense solar radiation, and moderate
Stickle 1980), presence of predators (Richardson and
wave action during tidal exchanges (Watanabe 2002). By
Brown 1992), and wave action (Richardson and Brown
feeding quickly, S. haemastoma avoids most of the
1990). In addition, P. lapidosa shows a seasonal growth
hazards associated with extremely long handling times.
cycle (McCarthy 2001), so differences in energy value per
Stramonita haemastoma survives and feeds on sab-
worm may also influence feeding rates and the amount
ellariid reefs despite the absence of its typical bivalve
of tissue ingested.
prey. Although S. haemastoma possesses feeding struc-
Shell-boring snails expend energy by scraping the
tures specialized for penetrating shells, a phenotypically
surface of a shell with their radula for hours or days. In
plastic proboscis as well as adaptable foraging strategies
addition, the production of enzymes used for the
allow this species to broaden its diet to include tube-
chemical dissolution of shells and wear and tear on the
dwelling polychaetes.
radula (Carriker 1978, 1981) are also costs associated
with boring. Because S. haemastoma on worm reefs do
not drill when feeding on tubeworms, there may be Acknowledgements We would like to thank Drs. J. Lin, R. Tank-
striking differences in the amount of energy required to ersley, and E. Irlandi for their many helpful comments and sug-
feed compared with conspecifics in other habitats. When gestions. We are grateful to Dr. G. Dietl and an anonymous
reviewer whose constructive criticism helped improve and
handling costs are low, prey become more profitable.
strengthen this manuscript. This paper is based on a dissertation
Most bivalves contain more tissue than P. lapidosa, but submitted by J. Watanabe in partial fulfillment of a PhD disserta-
comparisons of the amount of tissue ingested for every tion at Florida Institute of Technology. A Conchologists of America
hour of handling time allows meaningful comparisons of Graduate Fellowship, the Astronaut Trail Shell Club Scholarship,
and an HBOI Summer internship awarded to J. Watanabe, and
food values. Solitary S. haemastoma feeding on solitary
grants from the National Science Foundation awarded to C. Young
mussels (wet mass <2.0 g), clumped oysters (wet mass
provided financial support for the completion of this study.
$35.1 g), and solitary clams (wet mass $63.6 g), in-
gested 0.61, 1.48, and 0.34 mg DW hÀ1, respectively
(Brown and Richardson 1987). Snails feeding on P.
References
lapidosa are much more efficient, ingesting an average of
6.76 mg DW hÀ1 of handling time. Prey such as P. Bayne BL, Newell RC (1983) Physiological energetics of marine
lapidosa that provide relatively more return in a given molluscs. In: Saleuddin ASM, Wilbur KM (eds) The mollusca,
time period are, by definition, more optimal prey vol 4. Physiology Pt 1. Academic, New York, pp 407–515
Boggs CH, Rice JA, Kitchell RA, Kitchell JF (1984) Predation at a
(Hughes 1980). Feeding more efficiently can affect the
snail’s pace: what’s time to a gastropod? Oecologia 62:13–17
snail’s energy budget, and possibly manifest itself as
Brown KM (1997) Size-specific aspects of the foraging ecology of
changes in growth or reproductive output (Bayne and the southern oyster drill Stramonita haemastoma (Kool 1987).
Newell 1983). However, the energy contents of P. lap- J Exp Mar Biol Ecol 214:249–262
idosa and bivalve tissue need to be determined in order Brown KM, Alexander JE (1994) Group foraging in a marine
gastropod predator: benefits and costs to individuals. Mar Ecol
to make more meaningful comparisons. Despite saving
Prog Ser 112:97–105
time and energy, laboratory feeding experiments and Brown KM, Richardson TD (1987) Foraging ecology of the
field population studies have shown that shell-boring S. southern oyster drill Thais haemastoma (Gray): constraints on
haemastoma grow much more rapidly and attain much prey choice. J Exp Mar Biol Ecol 114:123–141
1029
Burrows MT, Hughes RN (1991) Variation in foraging behaviour McCarthy DA (2001) Life-history patterns and the role of distur-
among individuals and populations of dogwhelks, Nucella lapil- bance in intertidal and subtidal populations of the polychaete
lus: natural constraints on energy intake. J Anim Ecol 60:497–514 Phragmatopoma lapidosa lapidosa (Kinsberg 1867) in the
Butler PA (1985) Synoptic review of the literature on the southern tropical Western Atlantic. Dissertation, Kings College
oyster drill Thais haemastoma floridana. NOAA Technical McGraw KA, Gunter G (1972) Observations on killing of the
Report NMFS 35:1–12 Virginia oyster by the gulf oyster borer, Thais haemastoma, with
Carriker MR (1978) The chemical mechanism of shell dissolution evidence for a paralytic secretion. Proc Nat Shellfish Assoc
by predatory boring gastropods: a review and an hypothesis. 62:95–97
Malacalogia 17:143–156 Menge JL (1974) Prey selection and foraging period of the preda-
Carriker MR (1981) Shell penetration and feeding by naticacean ceous rocky intertidal snail, Acanthina punctulata. Oecologia
and muricacean predatory gastropods: a synthesis. Malacologia 17:293–316
20:403–422 Menge BA (1978a) Predation intensity in a rocky intertidal
Carriker MR, Van Zandt D (1972) Predatory behavior of a shell- community: relation between predator foraging activity and
boring muricid gastropod. In: Winn HE, Olla BL (eds) environmental harshness. Oecologia 32:1–16
Behavior of marine animals. Plenum, New York, pp 157–244 Menge BA (1978b) Predation intensity in a rocky intertidal com-
Dobberdeen RA, Pechenik JA (1987) Comparison of larval bio- munity: effect of an algal canopy, wave action and desiccation
energetics of two marine gastropods with widely differing on predator feeding rates. Oecologia 32:17–35
lengths of planktonic life, Thais haemastoma canaliculata and Padilla DK (1998) Inducible phenotypic plasticity of the radula in
Crepidula fornicata. J Exp Mar Biol Ecol 109:173–191 Lacuna (Gastropoda: Littorinidae). Veliger 41:201–204
Garton DW (1986) Effect of prey size on the energy budget of a Reid DG, Mak YM (1999) Indirect evidence for ecophenotypic
predatory gastropod, Thais haemastoma canaliculata. J Exp plasticity in radular dentition of Littoraria species (Gastropoda:
Mar Biol Ecol 98:21–33 Littorinidae). J Moll Stud 65:355–370
Garton D, Stickle WB (1980) Effects of salinity and temperature on Richardson TD, Brown KM (1990) Wave exposure and prey size
the predation rate of Thais haemastoma on Crassostrea virginica selection in an intertidal predator. J Exp Mar Biol Ecol
spat. Biol Bull 158:49–57 142:105–120
Gore RH, Scotto LE, Becker LJ (1978) Community composition, Richardson TD, Brown KM (1992) Predation risk and feeding in
stability, and trophic partitioning in decapod crustaceans an intertidal predatory snail. J Exp Mar Biol Ecol
inhabiting some subtropical sabellariid worm reefs. Bull Mar 163:169–182
Sci 28:221–248 Scheltema RS (1971) Larval dispersal as a means of genetic
Gunter G (1979) Studies of the southern oyster borer, Thais exchange between geographically separated populations of
haemastoma. Gulf Res Rept 6:249–260 shallow-water benthic marine gastropods. Biol Bull
Hughes RN (1980) Optimal foraging theory in the marine context. 140:284–322
Oceanogr Mar Biol Annu Rev 18:423–481 Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol
Hughes RN, Elner RW (1980) Tactics of a predator, Carcinus Syst 2:369–404
maenas, and morphological responses of the prey, Nucella Trussell GC (1997) Phenotypic plasticity in the foot size of an
lapillus. J Anim Ecol 48:65–78 intertidal snail. Ecology 78:1033–1048
Ingham RE, Zishke JA (1977) Prey preferences of carnivorous Trussell GC (2000) Phenotypic clines, plasticity, and morphological
intertidal snails in the Florida Keys. Veliger 20:49–51 trade-offs in an intertidal snail. Evolution 54:151–166
Janson K (1987) Allozyme and shell variation in two marine snails Vermeij GJ (1978) Biogeography and adaptation: patterns of
(Littorina, Prosobranchia) with different dispersal abilities. Biol marine life. Harvard University Press, Cambridge
J Linn Soc 30:245–256 Watanabe JT (2002) The ecology of the southern oyster drill,
Kirtley DW (1968) The reef builders. Nat Hist (NY) 77:40–45 Stramonita haemastoma (Gastropoda: Muricidae) on Florida
Liu LL, Foltz DW, Stickle WB (1991) Genetic population structure sabellariid worm reefs. Dissertation, Florida Institute of Tech-
of the southern oyster drill Stramonita (=Thais) haemastoma. nology, Melbourne
Mar Biol 111:71–79