235

EXPERIMENTAL STUDIES OF A BENTHIC PREDATOR-PREY

RELATIONSHIP. 1. FEEDING, GROWTH, AND EGG-COLLAR
PRODUCTION IN LONG-TERM CULTURES OF THE
GASTROPOD DRILL POLINZCES ALDERZ (Forbes)
FEEDING ON THE BIVALVE TELLZNA TENUZS (da Costa)

A. D. ANSELL
The Dunsrqffkage Marine Research Laboratory, Ohan. Arg,vll. Scotland

Abstract: Groups of naticid gastropod drills. Polbzicrs alderi (Forbes) were kept in constant temperature
laboratory culture, using the bivalve TeNirza rerwis (da Costa) as prey. for periods in excess of 2 yr,
to study rates of feeding, growth, and egg collar production. Following an initial growth phase. further
growth, egg production, and food consumption all showed a clear annual cycle of variation in those
cultures which contained both sexes. During the growth phase. growth rates varied with temperature
with the highest rates at 20°C; in this phase, temperature and predator size accounted for most of the
variation found in rates of predation and food consumption. During the reproductive phase, somatic
growth was small and showed no temperature dependence; in this phase, temperature and rate of egg
collar production accounted for most of the variation found in rates of predation and food consumption.
In single sex cultures there was no egg production but, in separate experiments, isolated mated females
continued to produce eggs >l yr after isolation. Maximum rates of egg production were found at
15-20 “C. The maximum reproductive potential. at I5 “C. was equivalent to IO times the mean tissue
mass during a single annual reproductive period. Neither the timing nor duration of the reproductive
period was significantly different at IO. 15 or 20°C. but there was no egg production at 25 “C.

INTRODUCTION

Gastropods of the family Naticidae are common predators in marine benthic

systems in most parts of the world. They feed mainly on bivalves, sometimes on
other gastropods, and rarely on other prey organisms (Jensen, 1951; Ziegelmeier,
1954; Ansell, 1961; Paine, 1963) by drilling a hole through the shell of the prey
and rasping out the tissue by use of the radula, leaving a characteristically-shaped
bored hole as evidence of their activities. The abundance of bored shells in natural
populations has frequently been used as a measure of naticid predation (Ansell,
1960; Masse, 1963, 1971, 1972; George, 1965; Reyment, 1966; Green, 1968;
Negus, 1975) but surprisingly in spite of their apparent advantage as experimental
animals, until recently few experimental studies of naticid predation had been made,
and relatively little was known of the quanti~tive relationships between naticid
gastropods and their prey, or of the effects of intrinsic and external factors on the
naticid-bivalve relationship. Recent comprehensive studies involving in situ
measurements of predation and growth in caged Palinices f~~~~icu~~spreying on
0022-098 I :82/0000-0000/$02.75 Q 1982 Elsevier Biomedical Press
236 A. D. ANSELL

Mya arenaria (Edwards, 1975; Edwards & Huebner, 1977) and exclusion experi-
ments designed to test the effect of Polinices predation on benthic community
structure (Wilse, 1980) have provided much interesting information on these factors
for one North American species.
The present study of the naticid-bivalve relationship forms part of a collaborative
research programme between workers at the Dunstaffnage Marine Laboratory,
Oban (Scotland) and the Station Marine d’Endoume, Marseille (France), and has as
a primary aim the provision of information on thermal tolerances and responses
of dominant species on the infauna of sandy sediments, as a background to assessing
possible effects of thermal pollution on the inshore marine fauna of the European
coastline. The overall programme is concerned with basic behavioural and other
aspects of the responses of benthic invertebrates of sandy sediments to temperature,
and the influence of geographical factors on these responses. It has involved a
series of comparative studies of temperature tolerances and responses for a variety
of organisms, mainly molluscs, from North Atlantic and Mediterranean popula-
tions. Experimental studies of the Naticidae were included to provide an
opportunity to assess temperature effects at the level of interspecies interaction in
an important, entirely benthic, predator-prey relationship. Observations made of
naticid species in relatively long-term laboratory cultures at the Dunstaffnage
Laboratory and the Station Marine d’Endoume, using similar techniques, have
provided much information on feeding, growth, and reproduction and on the
energetics and trophodynamics of the naticid-bivalve relationship. This paper,
which deals with feeding, growth, and reproduction in Polinices alderi (Forbes)
from Scottish waters, is the first of a series dealing with the main results of
observations on North Atlantic Polinices species at Dunstaffnage, while work on
the Mediterranean species at Marseille is being described elsewhere (Mace, 198la,
b, c).

METHODS

ANIMALS

P. alderi for use in the culture experiments were collected from a population at
Gullane beach on the south shore of the Firth of Forth. At low tide, the gastropods
move actively over the surface of the exposed sand near low water mark, and
individual animals were located by searching for the trails left during this activity.
The P. alderi were transported to the Dunstaffnage Laboratory where they were
individually weighed and measured. They were then divided into groups of three
snails of similar size, and four such groups were selected to be kept at each of three
temperatures: 10, 15, and 20 “C, the groups being selected so that at each
temperature there was as wide a range of size groups as possible represented. Each
animal within each group was individually marked for later identification. This
 BENTHIC PREDATOR-PREY RELATIONSHIP 237

main group of cultures was set up on 22 July 1977. Later, attempts were made to
set up similar cultures at 25 “C and one group of animals was kept successfully at
that temperature, but for a more limited period,

CULTURE CONDITIONS

Each group of three P. aideri was placed in an individual small aquarium within
which was a sand bed into which the gastropods and their prey could burrow.
The sand bed consisted of washed, well-sorted beach sand, resting on a nylon
gauze above a layer of crushed shell, which in turn rested on a layer of coarse
stony gravel. The sea water was continuously re-circulated through this sediment
bed by means of a small air lift pump ensuring that the sand remained completely
oxygenated. The top of the aquarium was covered to minimize evaporation of the
sea water and to prevent escape of the gastropods and thus the cultures were
normally in darkness except for the periods when the water was changed or other
observations carried out. Thirty individuals of the bivalve Tel&a cenuis (da Costa),
collected from the beach at Gullane, or from other Scottish beaches, were added
to the sand in each aquarium as prey. The cultures at 10 and I5 “C were kept in
constant temperature cold-rooms at these temperatures, and those at 20°C in a
thermostatically-controlled water bath within the 15 “C cold-room. The 25 “C
culture was maintained under similar conditions in a thermostatically-controlled
water bath within the laboratory aquarium.
Each culture was examined at 2-wk intervals, when the sand was sieved to remove
both predators and prey, and all bored shells removed and replaced by living Tellinn.
In the process, the sea water was also completely changed. At 6-wk intervals, the
Polinices alderi were individually measured and weighed before being returned to
the culture tanks. P. alderi produces its egg masses in the form of a characteristic
collar, moulded by the foot from sand grains held together by mucus in which the
individual egg capsules are embedded. The c.ollars, produced in the sand, are
placed on the sand surface when completed. During most periods when egg collars
were produced, the cultures were individually examined at shorter intervals, often
daily, without disturbing the sand bed, and all egg collars were removed from each
cuhre and weighed after being lightly blotted dry.

MEASUREMENTS

The bored bivalve shells removed from each culture were measured, and the
weight of Tellina temis tissue consumed during each period for each culture was
then determined by conversion from the individual shell lengths using shell length-
dry tissue wt relationships for the Te&na used as prey. Food collsumpiion is
expressed here as dry wt of Tellina tissue consumed per unit time per Polinices.
In making this assessment, shells which were drilled but not consumed were not
included. The rate of growth of individual P. afd<>riwas determined as the increment
238 A. D. ANSELL

of shell height (measured from the base of the aperture to the top of the spire)
between sampling dates (normally a 6-wk period), and as the increment in total
fresh wt per Polinices between sampling dates. For evaluation of equivalent dry
tissue wt for P. alderi, a value of 107; of the total fresh wt has been used, based on
measurements of the actual dry tissue content of well-fed P. alderi in separate
cultures. Shell wt and total fresh wt for P. alderi were independently determined
to have the following relationship with spire height (H) for animals from the
Gullane population :

log total wt (mg) = 2.767 log H (mm) - 0.119 (1)

and
log shell wt (mg) = 2.717 log H (mm) - 0.240 (2)
There was no significant difference between the slopes of these relationships, and
over the range of size examined the mean shell wt expressed as a percentage of the
total fresh wt was 67.1%. The organic content of the shell, as determined by ignition
at 500_5lO”C, was 2.55% I?I0.06 SD.
For conversion of the weights of egg collars to equivalent organic content, a
number of freshly collected egg collars were first oven-dried and then ignited
at 500-510 “C, and the ash-free dry wt (representing organic content) determined.
The mean ash-free dry wt was 1.574 + 0.072’;; of the total fresh wt. As the sand
incorporated into the egg collars during their production has already some organic
matter attached, however, this conversion factor was corrected by deducting a mean
value for the organic content of sand in the culture tanks of 0.399 + 0.041”,,, to
give a corrected conversion factor of 1.175”,,. There were no differences either in
organic content of the egg collars or of the sand between cultures at different
temperatures,

MORTALITY AND TERMINATION OF THE CULTURES

Of the original 12 P. alderi at 10 “C, two (both from the group of smallest
individuals) died during the first 6-wk period. They were not replaced, and this
culture was continued with only a single individual. Another Polinices died in
November 1977, and thereafter until November 1979, which is the end of the period
to which the results in this paper refer, there was no further mortality at 10 “C.
At 15 “C, there was no mortality until January 1978 when @ne .Polinices in
Culture 2 died. A second in Culture 2 died in February 1978 and another, in
Culture 5, in March 1978. The survivors from these two cultures were combined
in June 1978. In Culture 1I, individuals died in August and October 1978 and the
survivors from this culture were combined with those of 2 and 5 in November 1978.
In Culture 8, the first death was in August 1978, the second in September 1979
and the third in November 1979, by which time only two of the original 12 animals
were surviving at this temperature.
 BENTHIC PREDATOR-PREY RELATIONSHIP ‘39

At 20°C there was no mortality until January 1978, when one individual in
Culture 6 died. One individual in Culture 3 died in May 1978 and the survivors
from Cultures 3 and 6 were then combined. Individuals died in Culture 9 in
May 1978 and October 1978 and the survivor from this culture was combined with
those from 3 and 6 in November 1978. Of these animals, one died in August 1978
and one in March 1979. The original three animals in Culture 12 survived until
May 1979 when a failure of the thermostat controlIing the 20°C cultures resulted
in their untimely termination.
An attempt was made to set up cultures at 25 “C in June 1978. P. alderi is close
to its upper Rmperature tolerance limit at this temperature and most of the animals
survived for only a short period. Three survivors were combined in a single culture
in September 1978 and there was no further mortality until May 1979 when one
individual died. The remaining two Polinices survived until November 1979 when
the culture was terminated.

RESULTS

CYCLICAL PERIODICITY IN REPRODUCTION, GROWTH, AND FEEDING ACTIVITY

DURING THE CULTURE PERIOD

The basic results for each individual culture are summarized in Figs. I and 2
which show the weights of Tellina tissue consumed, the total weight increments for
Palinices alderi, and the numbers of egg collars produced, for each period for each
culture.
All the cultures showed certain features in common. Following their establish-
ment, there was an initial period when no egg collars were produced, during which
most of the Polinices grew rapidly; in most cultures this was accompanied by
initially high rates of consumption of Tel~jna tenrris w-hich then declined. Following
this period - referred to as the initial growth phase - growth rates declined, and
in most cultures egg collars were produced. The rate of egg-collar production
showed a consistent pattern of cyclical fluctuation, so that in the longest surviving
cultures there were two cycles of reproductive activity - the reproductive phases -
with a circum-annual periodicity leading to maximum rates of egg production in
May-June and minimum rates in October-November (Fig. 1). The numbers of
T. i~fl~l~,~,
and consequently the weight of TeI~~~a-tissue consumed rose rapidly as
egg-collar production increased, to a maximum rate coinciding with the maximum
rate of spawning, and fell as egg-collar production fell. In a few cultures there
continued to be no egg-collar production after the initial growth phase, and these
were interpreted as cultures in which the P~~inj~~s were either all females or all
males; in P. aldwi sex discrimination by external examination is not possible, and
consequently the initial selection of the gastropods could take no account of sex.
In contrast to the mixed-sex cultures. the single-sex cultures showed no consistent
240 A. D. ANSELL

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 BENTHIC PREDATOR-PREY RELATIONSHIP 241

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Fig. 1. Po&tzic~s alderi: histogram, mean growth increments as mg total wt -6-wk-‘; 0, egg-collar
production as no. .6-wk -I . Polinices- ’ , l , food consumption as mg dry Tell&a-tissue .6-wk-’ f
Pofinices- ; mixed-sex cultures maintained at 10, 15, and 20°C; the numbers refer to individual
cultures; *, individual mortalities.

cyclical patterns of fluctuation in rate of consumption of Tellina (Fig. 2), although

with the exception of the single individual at 10 “C (Culture 10) these cultures were
not maintained for as long a period.
Of the four 10 “C cultures, three were mixed-sex cultures, the other consisting of
a single individual only. The results for the three mixed-sex cultures are summarized
in Fig. 1. In all three cases the initial growth phase lasted for x 18 wk during
which there was no egg production except for a short period at the start in
Culture 1. The main period of egg-collar production began during December 1977
and the rate then increased to reach a maximum during the period April-June 1978.
Egg-collar production then declined: in Cultures I and 4 to zero in October-
November, and in Culture 7 to a minimum in October, but without a complete
stop. Following a period of low or zero egg production, there was a renewed
increase in the rate of egg production to a second maximum in May-June 1979
followed by a second decline. Thus, in all three cases at 10 “C, where most of the
initial animals survived together in culture for a period in excess of 27 months,
the circum-annual periodicity of rates of egg production was clearly shown.
242 A. D. ANSELL

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Fig. 2. Po/bric,c~.s u/&i: histogram. mean growth increments as mg total wt .6-wk-‘; 0. egg collar
production as no. .6-wk -’ . Polinices ’ , l , food consumption as mg dry TGncr-tissue .6-wk -’
Polinieta-‘: single-sex cultures nlaintained at 10. 1.5, and 20°C. and a single culture at 25-C; the
numbers refer to individual cultures; *, individual mortalities.
 BENTHIC PREDATOR-PREY RELATIONSHIP ‘43

Three cultures at 15 “C began as mixed-sex cultures; numbers 2, 8 and 11 (Figs. 1

and 2). No egg collars were produced during the initial growth phase except for a
short period at the start in Culture 2. The 15 “C cultures showed the greatest
variability in the timing of the subsequent first production of egg collars: in
Culture 8, production started in mid-October; in Culture 2, in late October; and
in Culture 11, in late November. Following mortality of two animals in Culture 2.
egg production ceased, but in Cultures 8 and 11 the rate of egg production continued
to increase. to reach maximum rates in May. As at 10°C. this was followed by a
decline in rate, to zero in Culture 11 (although this coincided with mortality of
two animals) and to a minimum rate in October in Culture 8. In Culture 8 this was
then followed by a renewed increase in the rate of egg production, in a second
cycle of reproduction. although with a less clearly defined seasonal maximum.
At 20°C. two cultures were mixed-sex (Fig. 1). The initial growth phase lasted
for z 18 wk and the first egg collars were produced in November. Both cultures
showed a first cycle of reproductive activity similar to those observed at 10 and
15 “C, while Culture 12. in addition. showed the first stages of a second cycle
before being terminated by an accident.
The failure of the remaining cultures at 15 and 20 “C to produce egg collars
(Fig. 2) is taken as evidence that they were set up with only one sex represented.
This view is supported by the results of combination of survivors from such cultures.
At 2O”C, the survivors of Cultures 3 and 6 were combined, and at 15 “C the
survivors of Cultures 2 and 5 were combined; in both cases this resulted in the
immediate production of egg collars.
The single culture of survivors at 25 “C showed no egg collar production (Fig. 2).
The rate of consumption of Tcllina also remained relatively constant at this
temperature.

SOMATIC GROWTH

Polinicrs alderi in cultures showed the greatest growth increments during the
initial growth phase. Rate of growth was reduced during the reproductive period,
but there was some indication of a second minor growth phase in some cases
preceding the second increase in egg production.
During the growth phase, shell height increments were variable, but generally
greater, than those made during the reproductive phases, at all three temperatures.
Regressions fitted to Ford-Walford plots of shell spire-height increments provide
the following relationships:
During the growth phases :

at 10 “C, k2 = 0.935 h, + 1.017

at 15 “C, /I? = 0.826 h, + 2.388
at 20 “C, 11~= 0.770 h, + 3.764
at 25 “C, h, = 0.829 h, + 2.253
244 A. D. ANSELL

During the reproductive phases:

at 10 “C, h, = 0.963 h, + 0.643

at 15 “C, h: = 0.896 h, + 1.725
at 20 “C, k, = 0.923 h, + 1.322

where /I, and hz are shell spire heights for individual P. alderi at successive 6-wk
intervals. During the growth phases growth rate was related to temperature: the
highest increments were found at 20°C and the lowest at 10 “C. During the
reproductive phases, increments were smaller at all temperatures (Fig. 3A) and the
relationship to temperature was not so pronounced.
During the growth phase, there was a trend for the percentage growth increment
at all temperatures to decline with increase in size. The maximum size reached
after the first growth phase was related closely to the initial size of the animals
placed in the cultures, so that individual animals, or the animals in an individual
culture appeared to grow towards widely differing maximum lengths or weights
(L, or W,). This effect was briefly discussed elsewhere (Ansell & Mace, 1978).

A
3-l

phase

“$V 25 0 10 15 20 25

OC OC

Fig. 3. Po/i/~ir~.~ aldrri: mean growth increments, based on regressions Fitted to Ford-Walford plots of
increments of shell spire height for all cultures; A, short-term increments, during 6-wk periods of
“growth phases” and of “reproductive phases”, B, annual increments: the increments are calculated
(as mm increment) for an individual of 5 mm initial spire height.

Renewed growth during second and subsequent growth phases, and continuous
small growth increments during the reproductive phases, however, resulted in most
individuals which survived, at all temperatures, approaching a similar maximum
size. The results of the Ford-Walford plots suggest a maximum size of z 17 mm.
The maximum sizes reached by individuals at each temperature were 16.9 mm
 BENTHIC PREDATOR-PREY RELATIONSHIP 245

at 10 “C, 16.5 mm at 15 “C, and 17.0 mm at 20 “C. Regressions were also fitted to
Ford-Walford plots of annual increments of shell spire-height, giving the following
relationships :

at 10 “C, Hz = 0.652 H, + 5.702

at 15 “C, HJ = 0.396 H, + 9.702
at 20 “C, Hz = 0.391 H, + 10.582

where H, and H2 are shell spire heights for individual P. alderi at successive annual
intervals. Fig. 3B shows the relationship of annual growth increments to tempera-
ture, based on these relationships.

EGG PRODUCTION

The range of rates of production of egg collars in cultures is summarized in

Table I. Because reproductive activity was cyclical, no mean rate of egg-collar
production typical of each temperature could be defined; the number of egg collars
produced per Polinices per week ranged from zero to a maximum rate which varied
with temperature and from culture to culture, with the highest short-term rates
recorded at 15 and 20 “C (Table I, Fig. 4A). Ansell & Ma& (1978) have noted from
preliminary results that the rates of egg-collar production found in these controlled-
temperature cultures resembles that found at similar temperatures in well-fed

TABLE I

Polinices alderi: summary of observations on egg production at constant temperatures in laboratory

cultures.

Egg-collar production

Production per annual cycle

Max.
Temp. Cycle average Larvae
Culture no. (“C) no. rate,wk-’ No. g fresh wt (thousands)
_~ ~_______
1 IO I 0.78 24 44.2 361
2 0.76 I4 24.7 202

4 10 I 0.33 I4 18.4 150

2 0.22 II 14.6 I19

7 IO I 0.38 II 11.4 93
2 0.38 I2 18.8 I53

8 15 I 1.72 61 91.7 747

I1 15 1 0.95 36 42.7 348

9 20 I 1.78 40 66.5 543

I2 20 I 0.72 22 20.5 167

Mean production yr _’ Polinices _ ’ 24.5 35.3 288

Mean production cycle- ’ female-’ 49 70.6 576
246 A. D. ANSELL

cultures subject to natural temperature fluctuations, and the later results from the
present series of cultures fall within the same range of values.
The number and total weight of egg collars produced for each reproductive cycle
indicating total annual reproductive potential, for each culture are summarized
in Table I. With the small number of results available it is not possible to draw
general conclusions, but the results indicate a maximum annual potential for
reproduction at 15 “C (Fig. 4B). The maximum annual production found is
equivalent to x 10 times the total mean dry tissue wt of the P. alderi during a
single annual reproductive period.

OiT---T+ 10 15 25 0 10 15 20 25

OC OC

Fig. 4. Palinices alderr: A, short-term maximum rates of production of egg collars in cultures at IO.
15, 20, and 25°C; B, the total production of egg collars per year for the same cultures; the numbers
refer to individual cultures; for Cultures 1. 4 and 7 rates for 1st and 2nd cycles are shown.

The mean wt of the egg collars produced in each culture during each 6-wk period
is shown in Fig. 5, where, to allow comparisons between collars produced by
different sized individuals, the mean wt per egg collar is divided by the mean wt of
Polinices. There was a general trend of first an increase and then a more gradual
reduction in the mean wt of egg collars during each reproductive cycle and, in
addition, a reduction in the mean wt of collars produced during the second cycle,
when compared with the frst. It is not known whether this reduction results from
a progressive decrease in reproductive effectiveness during the culture period as a
response to culture conditions or from a generally non-isometric relationship
between gonad wt (and hence brood wt) and tissue wt in P. alderi with increasing
size. The weights of collars produced by individuals of the same size or by the same
individual, may show wide variation, because although the egg collar diameter is
closely related to the shell diameter as a result of the moulding process during egg-
 BENTHIC PREDATOR-PREY RELATIONSHIP 747

collar production (Giglioli, 1955) the length of the spiral egg collar produced may
vary from < 1 complete coil to 2.5-3 coils,

0.2

o-1

I
0-o
1977 1978 1979
Fig. 5. Polinrcesaldwi: changes in mean egg-collar wt (expressed as a proportion of the mean wt of
Polir~icc~s in the culture) during the culture period. at 10. 15. and 20°C; the numbers and different
symbols refer to individual cultures.

A limited number of determinations were made of total numbers of larvae

hatching from known initial weights of egg collar. These provide a value of
8154 _t 602 larvae .g-’ fresh wt. and enable estimates to be made of the fecundity
of P. ulderi in culture, which vary (Table I) from 93 to 747 thousand larvae cycle-‘.
Assuming that overall the sex-ratio in the cultures was 1 : 1. the mean production
248 A. D. ANSELL

of egg collars per female in all cultures during a single annual reproductive cycle
was 49 egg cohars, producing 576 thousand larvae.
It is of interest to examine the rates of egg-collar production found in culture
in terms of the apparent rates of ovocyte development involved. At 1.5“C, where
the highest short-term rates of egg production and the greatest numbers and weights
of egg collars per annual reproductive cycle were found, egg collars were produced
at rates of up to 2 . Folinices-’ -wk-’ with a mean organic content corresponding
to 7-267, of the dry tissue wt of the parent Po~;n~c~~.~. No direct estimates of the
relative somatic and gonadal weights have been mdde for P. alderi, but it is unlikely
that the gonad and other associated organs associated with egg-collar production,
account for > IO-20:/,, of the total dry tissue wt, so that each egg collar appears to
represent a complete spawning. This would suggest that, at the time of maximum
egg production, the turnover rate of new generations of ovocytes in the ovary is
only 3-4 days, at I5 “C, with similar estimates of = 9 days at 10 “C and = 6 days
at 20 “C.

EGG PRODUCTION BY ISOLATED MATED FEMALES

The failure of animals in certain cultures to produce egg collars suggested that
continued production of egg cohars depends on renewed mating. Mated females
continue to produce eggs in isolation and, to establish for how long this would
continue, a number of individual P.nf&ri, separate from those of the main series
of cultures, were placed in individual cages. Of these individuals, three were found
to be females. These were kept in the aquarium at ambient temperatures in
continuously renewed sea water and their production of egg collars recorded. After
their complete isolation in July, all three individuals continued to produce egg
collars at an average rate of 0.29 collars -day-’ until the end of August. One female
then produced a further egg collar between the end of August and 18 September
and a final egg collar between IS September and 6 October. No further egg collars
were produced through the winter, and one female died in February, but both the
remaining Females subsequently produced egg collars in the following June, that
is z 1 yr after being isolated. The observations show that sperm from mating in
one season may be stored and used to fertilize eggs produced the following year.
The availability of sperm to fertilize the eggs is an essential perquisite for the
production of egg collars. This is indicated by (I) the failure of females in some
cultures to produce egg collars, and their subsequent immediate response when
placed together with males, and (2) the observation through more than two years’
experience of these and other cultures of Polirrices in the laboratory, during which
the majority of the egg collars produced were hatched, that on no occasion was
an egg collar containing infertile eggs produced. In particuIar, the egg collars
produced by isolated females, even 1 yr after separation from any possible contact
with a male, were all fertile.
 BENTHIC PREDATOR-PREY RELATIONSHIP 249

PREDATION AND FOOD CONSUMPTION

In all mixed-sex cultures, the numbers of Tellina, and the weight of Tellina-tissue
consumed, rose rapidly during the first part of the reproductive periods, the
maximum rates coinciding in timing with the peak rates of production of egg
collars (Fig. 1). Thereafter the rate of consumption fell as the rate of production
of egg collars also fell.
As the Polinices alderi in culture grew there was a tendency for larger individuals
of Tellina tenuis to be bored preferentially if available. As far as possible, T. termis
of the preferred size range were provided throughout. This resulted in predation
rates (number of prey bored per unit time) remaining more or less independent
of increase in size of the Polinices while food consumption increased. Variations
in predation rate in the cultures, therefore, are largely accounted for by two
factors; differences in temperature and in rate of egg-collar production. The
empirical relationships between rate of predation and these two factors derived
from the culture results were as follows:

at 10°C T = 12.81. G(B)-’ + 1.08

at 15°C T= 8.82. G(B)-’ + 3.76
at 20°C T= 8.71. G(B)-’ + 6.20
where T is the number of prey organisms (Tellina tenuis) consumed . Polinicesm’ .
42-day period-‘, and G(B)-’ is an index of egg-collar production, G being the

Fig. 6. Polinicrs alderi: the relationship between prey consumption (no. TeNina consumed 6-wk-’
P0linicr.r _ ’ ), temperature, and index of egg-collar production (see text), based on all cultures.
250 .A. D. ANSELL

total organic content of the egg collars produced during a period and B the mean
organic biomass of the Poliuices present during the period. These relationships
exclude periods when no egg collars were produced. If periods when no egg collars
were produced are included, the relationships become:
at 10°C. T= II.35 G(B)-’ + 1.68
at 15”C, T= 7.23 G(s))’ + 5.42
at 20°C. T= 7.68 G(B)-’ + 6.94

The resulting overall relationship between predation rate. temperature, and index
of egg-collar production during the reproductive phases may be shown as a response
surface (Fig. 6).
During the growth phase, food consumption index (IF) expressed as dry wt of
bivalve tissue consumed in a 42-day period as a proportion of the total initial wt
of Polinicrs, declined with increase in size of the Polinices, in line with the decrease
in percentage wt increment. During the reproductive phase there was relatively
little variation in the food consumption index with size and the main factors
affecting food consumption were rate of egg production and temperature. During
this latter phase the food consumption index was related to temperature and the
gonadal production index by the following relationships (excluding periods when
no egg collars were produced):

Fig. 7. Poliniw,~ u/~/wi: the relationship between food consumption index (mg T4;pwtissue consumed
h-wk-’ tng-’ total wt of Po/inicr.s in culture). temperature. and index ofegg-collar production (see text).
based on all cultures.
 BENTHIC PREDATOR-PREY RELATIONSHIP Xl

at 10 “C, IF = 0.2683 G(B)-’ + 0.0742

at 15°C W= 0.2233 G(B)-’ + 0.1560
at 20 “C, IF = 0.2566 G(B)-’ + 0.1774

The intercepts of these relationships provide an estimate of the mean rate of food
consumption for mature individuals ( >500 mg total wt) at each temperature
during periods when no egg collars were produced. At 25 ‘C where no egg collars
were produced the mean value of food coilsunlption was 0.2024 f 0.015 SD. The
resulting overall relationship between food consumption index, temperature, and
index of egg-collar production during the reproductive phase is shown in Fig. 7.

DISCUSSION

CYCLICAL PHENOMENA IN CULTURE

The most striking result from this series of long-term cultures is the appearance
of clear annual cycles of egg production in the mixed-sex cultures. The results
suggest strongly that there is an intrinsic annual cycle controlling growth and
reproductive activites in P. alderi, although the conditions of culture were not so
scrupulously maintained that the absence of environmental cues can be eliminated.
The P. alderi were buried in sand, in aquaria covered by opaque lids, contained
within controlled-temperature rooms without windows, and although there was
irregular artificial lighting, it seems unlikely that any light stimulus would affect
the cycle. Temperature was controlled within fairly narrow limits, except for the
periods at 2-wk intervals when both P. alderi and their prey were sieved from the
sand, and the water changed: no precautions were then taken to raise the replace-
ment water to the exact experimental temperature so that regular, although brief,
temperature changes did occur. Finally, the Tellina tenuis used as prey were collected
regularly from natural beach populatioIls and therefore showed the natural seasonal
fluctuations in tissue weight shown by this species (Ansell & Trevaflion, 1967).
The timing of the cycles of egg production are similar to those found in natural
populations. Although there is no detailed information on natural egg-collar
production by Polinices alderi, observations at Gullane beach, in the Firth of Forth,
and at Barassie, in the Firth of Clyde, over several years have shown that egg
collars are found only during the period May to September. Fretter & Shale (1973)
recorded the larvae of P. alderi in the Plymouth plankton mainly between May and
September indicating a similar cycle in that area. As in some of the controlled-
temperature cultures, P. alderi kept in cages in continuously renewed sea water at
normally fluctuating ambient temperatures, and with abundant food, at the
Dunstaffnage Laboratory, continued to produce egg collars throughout the year,
although at very slow rates during the winter (Ansell & Mace, 1978), indicating
that factors other than temperature are important in restricting the length of the
252 A. D. ANSELL

reproductive period in this species. Availability of suitable food is perhaps the

most important factor.

RATES OF PREDATION AND FOOD CONSUMPTION

At the time of peak egg-collar production in the present cultures the maximum
predation rate recorded was x 0.5 Tellina . day ’ . Polinices-’ averaged over a 6-wk
period, equivalent to a consumption index of ~0.6. At this rate of consumption
a Polinices ingests each week a wt of dry bivalve tissue approximately equivalent
to its own dry tissue wt, or x IS’?,, of body wt per day. When no egg collars are
produced this index drops to between 1.7”,, (at lO@C) and 4.8”,, (at 25 “C) of
body wt per day.
The rates of predation found in the experimental cultures are similar to those
which have been recorded from other naticid species in field and laboratory
experiments (Stinson, 1946; Wheatley, 1947; Hanks, 1952; Bernard, 1967; Green.
1968; Edwards, 1975; Edwards & Huebner, 1977; Mace, 1981a; Griffiths, 1981).
In the most comprehensive of such studies, involving field experiments with P.
duplicatus, Edwards & Huebner (1977) found that with a given, specified food
supply and experienced predators, i.e. predators previously accustomed to that
food supply, temperature was the key determinant of number of prey eaten, and
temperature and snail weight together accounted for most of the variability in
ingestion rates. Feeding rate varied directly with temperature with peak values
of 0.6 prey (hfJ,a arenmia) . snail-’ . day-’ in the warmest months, but ceasing
(at ~5 “C) for 4 months in winter. On a year-round basis ingestion rates were
only z I”;, of body wt .day-‘, and even during peak feeding (in summer) this index
was only 5-6”i,,, which compares closely with values found in our experiments
during non-reproductive periods.
Edwards & Huebner’s experiments were of two types, namely (a) year-round
experiments with individually caged Poliniccs duplicatus, and (b) short-term (6-wk)
summer-experiments with groups of five Poliuices. Neither, therefore, provided
conditions under which rates of egg production could be studied, and consequently
the results relate to growing animals, but give no information on the effects of
reproductive activity on predation rate or food intake. Most other experimental
studies of naticid gastropods have also involved short-term experiments and
similarly provide no information on the effects of reproductive activity.
In our laboratory cultures, where food was not generally a limiting factor, rates
of predation and food consumption seem generally to have been determined by
the energy and nutrient demands engendered by the reproductive, growth, and
maintenance requirements of the predator, indirectly affected by temperature, and
were greatly increased during the reproductive phases. In nature, except in
exceptionally favourable circumstances, food is less readily available so that food
availability acts as a limiting factor restricting predation rate and hence growth
and reproduction of naticids.
 BENTHIC PREDATOR-PREY RELATlONSHIP 253

REPRODUCTIVE ACTIVITY

The culture results suggest that in naticids the conflicting requirements for
somatic growth and reproduction are segregated both within the life span, and
within each annual cycle, so that somatic growth is restricted, first, to a juvenile
period before first sexual maturity, and then, following sexual maturity, to periods
recurring cyclically but limited by the reproductive period. This segregation forms
the basis, in P. alderi, for the efficient allocation of resources between somatic
growth and reproduction both within the life cycle as a whole and within each
annual period, so that, when food resources are limited, a proportion is still utilized
for gamete production, while somatic growth is reduced. When abundant food
resources are available, however, as in the culture experiments, P. alderi is able
to convert bivalve tissue rapidly into gametes. The high rate of egg production
found under these circumstances emphasizes the “opportunistic” nature of this
species as a predator, and its great potential for rapid exploitation of available
resources for population increase. It would be interesting to compare these rates
with information for other naticid species, particularly for those which show
different reproductive patterns, but this is not yet available. A recent survey of
reproductive effort in molluscs generally (Browne & Russell-Hunter, 1978), how-
ever, suggests that under normal conditions reproductive output varies between
z 0.15 and 2.4 times body wt per year for semelparous mollusc species, and z 0.06
and 0.4 times body wt per year for iteroparous species (expressed as the ratio
between the amount of carbon channelled into reproduction and the amount of
carbon contained in the average adult female). These values fall far short of the
maximum potential of x 10 times body wt found here in culture.
Preliminary observations on a second Polinices species in British waters, P.
catena, which has direct development of the juveniles in the egg collar at the
expense of nurse eggs, show much lower rates of egg-collar production than for
P. alderi, where the embryos hatch as pelagic veligers, but direct comparisons are
difficult because of logistic difficulties in maintaining adequate prey populations
with the larger naticid species. Further studies are necessary to provide reliable
comparative data on reproductive potential of P. catena.

EFFECTS OF TEMPERATURE

The effects of temperature on the factors investigated here in constant-tempera-

ture culture may be briefly summarized. Differences in temperature appeared to
have little effect on the timing or the extent of the reproductive period in mixed-sex
cultures; at 10, 15, and 20 “C the periods when egg collars were produced were
roughly similar and the timing of periods of maximum production show no
significant differences. During periods when no egg collars were produced, the
metabolic demand engendered by growth and maintenance as reflected in rates of
predation and food consumption increased with temperature in the range of
254 A.D. ANSELL

lo-2O”C, but was reduced at 25 “C. In the range lo-20 “C, the mean Q,, during
the growth phase was close to 2. During the reproductive phase, temperature
differences set limits to the maximum rates of egg production possible, with high
maximum rates at 15 and 20 “C compared with 10 “C where the gamete production
index never exceeded a value of 0.75. During this phase, somatic growth was slow
and showed less temperature dependence, but rates of predation and food con-
sumption reflected the differences in maximum rates of egg production; as a result,
values of Q,,, for these rates during the reproductive period were high. The results
indicated an optimum temperature for P. uldeeri in the range 15-20°C where rates
of growth and of egg production reach their highest values.

ACKNOWLEDGEMENTS

It is a great pleasure to acknowledge the skilled technical assistance of Miss Fay

Newman (Mrs. R. Harvey), without whose devoted care these cultures would not
have survived so long. The experiments were carried out as part of a project jointly
funded contract no. 225-77-l ENV UK by the Environment Fund of the Com-
mission for the European Communities, and the Natural Environment Research
Council. Many helpful discussions during the progress of this work, with Dr. H.
Mass6 and Mlle. A.-M. Ma& are gratefully acknowledged.

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