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Behavioural components of prey-selection by dogwhelks, Nucella lapillus (L.), feeding on barnacles, Semibalanusbalanoides (L.), in the laboratory
91
J. Exp. Mar. Biol. Ecol., 1984, Vol. 79, pp. 91-103
Elsevier
JEM 290
BEHAVIOURAL
NUCELLA
COMPONENTS
LAPILLUS
OF PREY-SELECTION
BY DOGWHELKS,
(L.), FEEDING ON BARNACLES,
BALANOZDES
SEMIBALANUS
(L.), IN THE LABORATORY
S. DE B. DUNKIN
and R.N. HUGHES School of AnimalBiology, University College of North Wales, Bangor, Gwynedd, LL57 2UW. U.K. Abstract: Adult dogwhelks, maintained on mussels for 60 days before experimentation to reduce prior effects of ingestive conditioning and handling skills appropriate to barnacles, and thence deemed “inexperienced”, preferred the largest barnacles presented to them. Juvenile and adult dogwhelks, maintained on barnacles and deemed experienced, preferred barnacles of intermediate sizes that were correlated with the sizes of the dogwhelks. “Inexperienced” dogwhelks penetrated barnacles significantly more often by drilling than by prising, whereas experienced dogwhelks did the reverse. A predominant tendency to prise open barnacles was developed by previously “inexperienced” dogwhelks after they had eaten six to eight consecutive prey. Larger dogwhelks prised open greater proportions of larger barnacles than did smaller dogwhelks. Experienced adult dogwhelks prised open all barnacles of %2-mm opercular diameter but only 20% of those x6 mm in diameter. The preferred barnacles, 4-5 mm in opercular diameter, were of a size that the experienced adult dogwhelks could prise open in 50% of attacks. Dogwhelks inspected barnacles by crawling over them for % 20 min when the prey were subsequently rejected and w 30 min when subsequently eaten. Penetration time and ingestion time were linear functions of barnacle diameter, total handling time ranging from 4-26 h for barnacles of 2.5-2.7 mm opercular diameter. Experienced dogwhelks handled barnacles faster than “inexperienced” dogwhelks, largely because they used the quicker method of penetration by prising whenever possible. The yield of flesh per unit handling time was an accelerating function of barnacle size and, with experience, could be increased by a factor of x 1.2 for barnacles of 7 mm opercular diameter to x 2.0 for barnacles of 2 mm opercular diameter. The preference of experienced dogwhelks for barnacles somewhat smaller than the largest available, may have reflected the greater frequency with which these prey could be penetrated by the quicker method of prising. Minimizing handling time could be important in nature if there is a risk to feeding dogwhelks of being displaced by competitors. In the laboratory, 12% of dogwhelks where thus displaced. Barnacles of x 5 mm opercular diameter were estimated to be slightly more profitable than mussels of x 17.5mm shell length to a dogwhelk experienced with barnacles, but less profitable to a dogwhelk that has recently fed extensively on mussels. Dogwhelks, therefore, might switch between diets predominately of barnacles or of mussels if prey of comparable protitabilities change drastically in their relative abundance on the shore.
INTRODUCTION Nucella lapillus feed selectively when offered different sizes of one of their principal prey, Myzilus edulis (Bayne & Scullard, 1978 ; Hughes & Dunkin, 1984a). This selectivity is enhanced as dogwhelks gain experience with prey, but the preferred size of mussel is somewhat less than that predicted to yield the most flesh per unit handling time if 0022-0981/84/%03.00 0 1984 Elsevier Science Publishers B.V.
92
S.DEB.DUNKIN
AND R.N.HUGHES
feeding is unconstrained by extraneous factors (Hughes & Dunkin, 1984a). Barnacles are the other principal prey of I&W&J Iapitlu;s(Moore, 1936; Connelf, 1961; Largen, 1967; Morgan, 1972; Menge, 1978) and the present investigation quantifies the foraging behaviour of dogwheiks presented with barnacles in the faboratory, with particular reference to size-selection, yield per unit handling time and the effects on foraging of hunger, experience and interference from conspecific competitors.
MATERIAL
ANDMETHODS
Nucella lapillus (L.) of the sheltered-shore
morph (Hughes & Elner, 1979) were collected in April 1979 and irregularly thereafter from a stone jetty adjacent to Bangor pier (Ordn~ce survey reference SH 585733), where they had access to a dense popuiation of Sem~ba~an~s ~a~a~~~es (I,.) but not to ~ytilu~~ e&&s (L.) (Hughes & Dunkin, 1984a). Semibahus baianoides were collected, as required throughout the year, fixed to small stones from mid-tide level at Penmon, Anglesey (SH 625788). Experiments were conducted at 12 + 1 “C in a 12-h photoperiod. Aquaria contained recirculating sea water, maintained at 32-34x, S. EXPT. 1,SIZE-SELECTION
Barnacles were presented in abundances that approximately equalized the surface area represented by each size-class. Numbers used, obtained by scraping excess barnacles from the stones, were 26-34 barnacles of 2 to 3-mm opercular diameter (rostra-cane axis), 6-12 of? to 4-mm, 4-8 of 4 to 5-mm, and 3-6 of 5 to 6-mm. Stones bearing the barnacles, together with a dogwhefk, were placed in a 0.2 x 0.4-m aquarium and the dogwhelk allowed to feed for 7 days, after which the opercdar diameters of the eaten barnacles were measured. This procedure was repeated for 20 dogwhelks of 5 to IO-mm shell height, 20 of 15 to 20-mm, and 20 of 25 to 30-mm, representing first year, second year, and adult dogwhefks, respectively, ail of which had been mantled on a diet of barnacles for 60 days and then starved for I4 days to standardize hunger levels prior to experimentation. A further 20 adult dogwhelks, maintained for 60 days on mussels before starvation and therefore deemed “inexperienced” with barnacles, were subjected to the experimental procedure. Later experiments (Hughes & Dunkin, 1984b) showed that the effect of ingestive conditioning to barnacles would not have been eradicated completeIy after 60 days feeding on mussels, so that “inexperienced” can be used only as a relative term in the present context. Twenty aquaria containing the standard numbers of barnacles on stones, but lacking dogwhelks, served throughout the experiment to estimate the rno~~ty of barnacles not caused by predation,
NUCELLA EXPT.
2, METHODS
FEEDING
ON SEMIBALANUS
93
OF ATTACK
A stone bearing numerous barnacles of different sizes was placed together with a dogwhelk in a 0.2 x 0.4-m aquarium. The barnacles were inspected daily for 5 days noting the sizes consumed and whether the dogwhelk had gained entry by drilling through the opercular skeletal plates, drilling through the occludent margins of the opercular plates, or by prising the opercular plates apart. The experiment was repeated four times for each of 10 dogwhelks of 5 to lo-mm shell height, 10 of 15 to 20-mm, and 10 of 25 to 30-mm, and was run once for each of 40 “inexperienced” 25 to 30-mm dogwhelks. Experienced and “inexperienced” dogwhelks had been fed for 60 days on barnacles and mussels respectively, then starved for 14 days prior to experimentation. Four stones, densely covered with barnacles, were placed together with IO marked dogwhelks in a 0.5 x 0.35-m arena, over which was suspended a 16-mm Bolex camera, with synchronized flash, driven by a time-lapse mechanism giving exposures at 3-min intervals and loaded with a 30.5-m film lasting 7-g days. Durations of foraging behaviours were measured by counting frames with the aid of an L-W International Photo-Optical Data Analyzer. Prey-handling behaviour, as discernible on the film, was categorized into inspection time, defined as the time elapsing between the initial encounter of a dogwhelk with a barnacle and either rejection of the prey or initiation of attack, and post-inspection handling time, defined as the time elapsing between initiation of attack and abandonment of the prey. Initiation of attack was recognized as the cessation of exploratory movements of the dogwhelk over the barnacles for 1 h, determined from the analysis of previous frames. Completion of penetration and commencement ofingestion could not be distinguished on the film. Ingestion time was, therefore, measured directly from dogwhelks consuming barnacles whose opercular plates had been removed before presentation (Expt. 4). Penetration time was estimated as the difference between predicted post-inspection handling time and ingestion time. Dogwhelks handling barnacles were sometimes invaded by competitors and the ensuing interactions were timed from the film. EXPT.
3, EFFECT
OF HUNGER
ON HANDLING
BEHAVIOUR
Barnacles presented were of 4 to 6-mm opercular diameter, other sizes having been scraped off the stones. Four batches of 10 adult dogwhelks were starved for 0, 14,30, and 90 days prior to experimentation. Five dogwhelks from each of two starvation regimes were introduced into the arena and filmed. Four films were taken, covering all 40 experimental dogwhelks. Inspection time, post-inspection handling time and competitive interactions were measured from the films. EXPT.
4, EFFECT
OF EXPERIENCE
ON HANDLING
BEHAVIOUR
The natural covering of barnacles on the stones was used, incorporating barnacles of 2.0 to 7.5~mm opercular diameter. The opercular plates of ~40 barnacles were prised
94
S. DE B. DUNKIN
AND R.N. HUGHES
apart to allow dogwhelks immediate access to the flesh, so that ingestion time could be measured. Dogwhelks deemed experienced had been maintained solely on barnacles for 60 days and then starved for 14 days to standardize hunger levels prior to experimentation. Dogwhelks deemed “inexperienced ” (see Expt. 1 above) had been maintained solely on mussels for 60 days before starvation. Five experienced and five “inexperienced” dogwhelks were introduced into the arena and filmed. Eight films, covering 40 experienced and 40 “inexperienced” dogwhelks, were taken. Inspection time, post-inspection handling time, ingestion time, and competitive interactions were measured from the films. Penetration time was estimated from the predicted postinspection handling time and ingestion time. YIELD
OF FLESH FROM A BARNACLE
Dogwhelks consumed all the flesh of each barnacle attacked. The flesh of different sized barnacles was dissected from the exoskeleton, dried at 70 “C for 72 h and weighed. Barnacle dry flesh weight was related to opercular diameter by regression analysis. RESULTS EXPT.
I, SIZE-SELECTION
The size-frequencies of dead barnacles in the experimental aquaria were significantly different from those in the control aquaria (Fig. la,b, Log Likelihood Ratio, G = 162.7, d.f. = 3, P < 0.001) and the numbers of undrilled dead barnacles were significantly greater in the control aquaria (G = 36.2, d.f. = I, P < 0.001). Successively larger experienced dogwhelks preferred successively larger barnacles (Fig. Ic-e), although only the means for the smallest and largest dogwhelks were significantly different by Mann-Whitney U-test (Fig. 1, legend). The mean size of barnacles eaten by “inexperienced” dogwhelks was significantly larger than that for experienced ones (Fig. le,f). EXPI‘. 2. METHODS
OF ATTACK
“Inexperienced” dogwhelks penetrated barnacles significantly more often by drilling than by prising, whereas experienced dogwhelks did the reverse (Table I), Previously “inexperienced” dogwhelks developed a predominant tendency to prise open barnacles after six to eight consecutive prey had~been eaten (Fig. 2). The proportion of barnacles prised open depended upon the relative sizes of the predator and prey, larger dogwhelks prising open higher proportions of larger barnacles than did smaher dogwhelks (Fig. 3). EXP’I.
3, EFFECT OF HUNGER
ON HANDLING
BEHAVIOIJK
Hunger had no significant effect on inspection time (ANOVA, F = 1.OO,d.f. = 3.40, P > 0.35) or on post-inspection handling time (F= 1.53, d.f. = 3.34, P > 0.2).
NUCELLA
95
FEEDING ON ~~~IBALA~US
d 5 -IO
dogwhelks X-30
mm
degwhetks IS-20 mm
f r dogwhelks
mm
25-30 nm
~ 2
4
6 Opercutar
2 diameter
[mm]
4
I 6
Fig. 1. a, size-specific mortality rates of barnacles in the control aquaria; b, size-specific mortality rates of barnacles in aquaria containing dogwhelks of 25 to 30”mm shell height; c, d, e, size-frequencies of barnacles eaten by experienced dogwhelks; f, size-frequencies of barnacles eaten by “inexperienced” dogwhelks; histograms c-f each represent 20 barnacles consumed by 20 dogwhelks; Mann-Whitney U-tests of raw data for differences between mean sizes ofbarnacles eaten were: c with d, U = 145.5, P > 0.05; d with e, U = 148, P > 0.05; c with e, U = 95, P < 0.05; e with f, U = 114, P < 0.05.
S. DE B. DUNKJN AND R.N. HUGHES
96
Numbers of barnacles prised or drilled by adult dogwhelks that bad prcv~ously been fed on barnacles (experienced)or mussels (“inexperienced”) for 60 days before the feeding trials: Fisher exact probability test, P c a.001
_,
. . _...~._. -.
Experienced
**Inexpe~ence~
. Prised
26
?
Drilled
2u
R?
0
2
4
No. consecutive
6
8
-_
10
prey eaten
of
Kg. 2. The percentage of attacks made by 20 previously naive dogwhelks, involving drilling the skeletal plates (----), drilling of the opercular occludent margins (, . . .), prising of the opercular plates (). plotted against the cumulative number of barnacles eaten per dogwheIk.
91
FEEDING ON SEMIBALANUS
NUCELLA
a
100
l--l
dogwhelks S-10
mm
60
100
“r
25-30 mm
t 60 i
20
3.0 Opercular
50
k0 diameter
[mm
60
I
Fig. 3. The frequencies with which barnacles in successive size-categories were prised open by experienced dogwhelks (a, b, c) and “inexperienced” dogwhelks (d): each histogram represents 40 barnacles.
EXPT. 4, EFFECT OF EXPERIENCE
ON HANDLING
BEHAVIOUR
Inspection time was significantly longer prior to the attack (29 +_2 min (SE)) than to the rejection (19.8 + 2 min (SE)) of a barnacle (F = 37.78, d.f. = 1,282, P < O.OOl),but was not significantly correlated with barnacle size (F = 0.56, d.f. = 4, 282, P > 0.65). Experience had no significant effect on inspection time either prior to the attack (F = 0.78, d.f. = 9, 124, P > 0.35) or to the rejection of a barnacle (F = 0.33, d.f. = 1, 122, P > 0.55). Inspection time was significantly shorter in the presence of competitors
98
S. DE B. DUNKIN AND R.N. HUGHES
prior to the attack (21 & 2 min (SE), F = 10.11, d.f. = 1, 159, P < 0.01) but not prior to the rejection of a barnacle (F = 2.03, d.f. = 1, 122, P > 0.5s). Post-inspection handling time was correlated with barnacle opercular diameter and was significantly longer for “inexperienced” than for experienced dogwhelks (Fig. 4). 0 0
0
0
O
0
.
0
16
l cl
0
.
0
12
8
4
0 2
3
4 Opercular
5 diameter
6
7
[m ml
Fig. 4. The time taken for adult dogwhelks to penetrate and ingest barnacles, plotted against size of the prey: 0, experienced dogwhelks; 0, “inexperienced” dogwhelks; the lines were derived from regression equations fitted to the data (see text).
Regression equations (2 SE) fitted to the data were: “inexperienced” dogwhelks, y = (1.08 + 0.09) x + (5.17 + O.l6), n = 53, PC 0.001, experienced dogwhelks, y = (1.59 F 0.11) x + (4.01 +_O.lS), n = 65, PC 0.001,where y = log, (postinspection handling time, min) and x = log, (barnacle opercular diameter, mm). The slopes of the regressions were Significantly different (I= 2.60, d.f. = i 15, P -=z 0.02).
Ingestion time was correlated with bamacle 0~~~~~ diameter (Fig. 5) but there was no si~c~t ~~~en~e between the slopes (t = 1.89, d.f. = 25, P > 0.05) ortheintercepts (t = 2.04, d.f. = 25, P > 0.05) of regressions for experienced and ‘~inexpe~enc~~’ dogwhelks. Pooled data were fitted by the regression: y = (162.1 + 19.5) 1, where y = ingestion time (min) and x - (124.4 + 10lS), n = 29, P -K0.00 x = barnacle operctiar diameter (mm).
01 2
L
t
L
Opercular
1
8
6 1mm f
I
diameter
Fig. 5. Time taken for adult do~helks
to ingest the flesh of barnacles whose opercular plates had been prised open before presentation, plotted against size of the prey: 0, experienced do~helks; 0, ~inex~~enced~ do~helks; the line represents the regression equation fitted to the pooled data (see text). 12 .
a 0 0 0
ru ? .r_ E
0
0 .
8
0 0
2
3
0
a 00
o”
L
5
6
0
7
8
Oparcuiot diameter In& Fig. 6. Time taken by adult do~helks to penetrate barnacfes by drilhng (0) or prising (a), plotted against size of the prey: the lines represent regression equations fitted to the data (see text).
l(W)
S. DE B. DUNKIN AND R.N. HUGHES
Penetration time was an approximately Iinear function of bamacie opercular diameter over the range of prey sizes used and was significantly longer when penetration was by drilling than by prising (Fig. 6). Regressions fitted to the data were: drilhng: v = (64.7 + 15.2) x - (75.9 + 92.11, n = 78, P < 0.005, prising: f: = (47.7 * 12.3) X - (106.8 + 62.5), n = 40, P < 0.00’7, where y = penetration time (min) and .X= barnacle opercular diameter (mm). The slopes of the regressions were significantly different fb = 2.32, d.f. = 114, P < 0.02).
2
3 Opercular
4
s
6
diameter Imml
Fig. 7. The time eiapsing between the arrival of an intruding dogwhelk at a barnacte already being handled by another dogwhelk and the departure of one of the dogwhetks, ptotted against size of the prey.
12 y0 of feeding dogwhelks were displaced by competitors. The duration of competitive encounters between intruding dogwhefks and the original occupants of barnacles was negatively correlated with barnacle size (Fig. 7) and was described by the regression equation: y = ( - 1.88 + 0.77) x I- (30.19 + 4.33), n = 26, P - 0.01, where y = encounter duration (min) and x = barnacle opercuiar diameter (mm).
101 YIELD OF FLESH FROM A BARNACLE
Barnacle dry flesh weight was related to opercular diameter by the regression equation: y = (3.61 2 0.34) x - (4.06 k 0.47), n = 52, P < 0.001, where y = log, (dry flesh weight, mg) and x = log, (opercular diameter, mm).
DISCUSSION
Dogwhelks previously maintained on mussels and assumed to have lost some of the effect of ingestive conditioning (Wood, 1968) or of temporarily developed handling skills (Hughes & Dunkin, 1984a) for barnacles, preferred the largest barnacles offered. Preference for the largest barnacles available has also been recorded in dogwhelks freshly collected from a shore where they had already been feeding predominantly on barnacles (Barnett, 1979). The West North American species, Thais lumellosa and T. canuliculutu, have been reported to prefer the larger barnacles among those available (Connell, 1970; Dayton, 1971), although Semibalunus curiosus may reach a threshold size at which it becomes less attractive or even immune, to dogwhelks (Dayton, 197 1). In the present investigations, however, dogwhelks that had gained experience feeding on barnacles shifted their preference to prey somewhat smaller than the largest available. This behaviour is not predictable from the potential profitability of the prey (yield of flesh/total handling time), which is an increasing function of barnacle size (Fig. 8). Time taken for prising is about 0.53 times that for drilling barnacles of 2-mm opercular diameter and about 0.64 times that for drilling 6-mm barnacles (regressions, Expt, 4). By changing from drilling to prising, dogwhelks increase the profitability of prey (Fig. 8) by a factor of sz 1.2 for barnacles of 7-mm opercular diameter to z 2.0 for 16-
‘; .:
12-
28
0'
0
1
I
I
I
2
L
6
8
Opercular
diameter
[ mm 1
Fig. 8. Profitability of barnacles to adult (25-30 mm) dogwhelks, calculated as (dry weight of ingested flesh)/(inspection + penetration + ingestion time) using regression equations given in the text, plotted against prey size for experienced (upper curve) and “inexperienced” (lower curve) dogwhelks.
102
S. DE B. DUNKIN
AND R.N. HUGHES
barnacles of 2.5mm. Larger barnacles, however, become harder to prise open, the proportion prised by experienced dogwhelks falling from 100% for barnacles of 2-mm opercular diameter to x 20 7; for those of 6-mm (Fig. 3). Dogwhelks preferred sizes of barnacles that they could prise open with z 50% chance of success. But even allowing for the lower probability that larger barnacles will yield to prising, their average profitability is still greater than that of smaller barnacles. Emlen (1966, discussed in Hughes, 1980) found that Thais emurginata preferred barnacles smaller than the largest available and demonstrated that the profitability of the largest Semibalanus cariosus could be devalued by x 307; when competing dogwhelks interfered with the handling of prey and stole flesh. Consequently, the average protitability of the largest was less than that of smaller S. cariosus, perhaps explaining the size-selection by Thais emarginata. In .the present study, Nucella lapillus were displaced by “interlopers” in 12% of cases while handling Semibalanus balanaides, compared with 61 y0 while feeding on Mytilus edulis (Hughes & Dunkin, 1984), probably reflecting the difference in prey size. “Interlopers” are able to steai flesh by gaining entry through the gaping valves of a mussel that has already been drilled (Hughes & Dunkin, 1984a). Similarly, in the case of large Semibalanus cariosus, there is room for several interloping Thais emarginata to drill and steal flesh from the original occupant (Emlen, 1966). Semibalanus balanoides, however, is too small for more than one dogwhelk to handle simultaneously, with the result that interlopers could devalue the prey item only by prolonging handling time or by displacing the original occupant. Interlopers did not significantly lengthen handling time (Expt. 4). Displacement by an interloper, on the other hand, could be seriously disadvantageous if it occurred long after the original occupant had begun its attack on the barnacle. Inspection and penetration time together ranged from z 45 % of total handling time for barnacles of 2-mm opercular diameter to x 30 % for those of 6-mm opercular diameter (regressions, Expt. 4). Connell (1970) estimated that Thais larnellosa spent NN 70-80% of total handling time penetrating Semibalanus curiosus. There is, therefore, a chance that dogwhelks may be displaced even before any flesh has been ingested. Total handling time for Nucella lapillusfeeding on Semibalanus balanoides ranged from 4-26 h (regressions, Expt. 4) and was estimated to be x 2 1.7 h from the data of Connell (196 l), leaving little time during high tide, when dogwhelks are active (Connell, 1961, 1970) for a displaced dogwhelk to attack another barnacle. A tidal constraint on foraging time, together with risks from competitors, could devalue the average profitability of larger barnacles estimated on the assumption of unhmited foraging time. We can offer no explanation for the size-selection other than being a means of maximizing the yield of flesh within the constraints imposed by the risk of competition in a limited foraging period, or a means of minimizing the time spent foraging, during which a dogwhelk could be at risk to predation, dislodgement by waves or desiccation.
NUCELLA
FEEDING ON SEMIBALANUS
103
ACKNOWLEDGEMENT
We gratefully acknowledge the support of NERC grant GR3/3695.
REFERENCES BARNE’IT,B.E., 1979. A laboratory study of predation by the dogwhelk Nucella lapillus on the barnacles Elminius modestus and Balanus balanoides. .l. Mar. Biol. Assoc. U.K., Vol. 59, pp. 299-306. BAYNE,B. L. & C. SCULLARD,1978. Rates of feeding by Thais (Nucella) lapillus(L.). J. Exp. Mar. Biol. Ecol., Vol. 32, pp. 113-129. CONNELL,J.H., 1961. Effects of competition, predation by Thais lapillus and other factors on natural populations of the barnacle Balanus balanoides. Ecology, Vol. 42, pp. 710-723. CONNELL,J. H., 1970. A predator-prey system in the marine intertidal region. I. Balanus glandula and several predatory species of Thais. Ecol. Monogr., Vol. 40, pp. 49-78. DAYTON,P. K., 1971. Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr., Vol. 41, pp. 351-389. EMLEN,J.M., 1966. Time, energy and risk in two species of carnivorous gastropod% Ph.D. dissertation, University of Washington, Seattle, 112 pp. HUGHES, R.N., 1980. Optimal foraging theory in the marine context. Oceanogr. Mar. Biol. Annu. Rev., Vol. 18, pp. 423-481. HUGHES, R.N. & S. DE B. DUNKIN, 1984a. Behavioural components of prey selection by dogwhelks, Nucella lapillus(L.), feeding on mussels+Uytilus edulis L., in the laboratory. J. Exp. Mar. Biol. Ecol., Vol. 77, pp. 45-68. HUGHES, R.N. & S. DE B. DUNKIN, 1984b. Effect of dietary history on selection of prey, and foraging behaviour among patches of prey, by the dogwhelk, Nucella lapillus (L.). J. Exp. Mar. Biol. Ecol., Vol. 79, pp. 159-172. HUGHES, R.N. & R. W. ELNER,1979. Tactics of a predator, Carcinus maenas, and morphological responses of the prey, Nucella lapillus. J. Anim. Ecol., Vol. 48, pp. 65-78. LARGEN,M. J., 1967. The diet of the dog-whelk, Nucella lapilh (Gastropoda : Prosobranchia). J. Zool., Vol. 151, pp. 123-127. MENGE, B.A., 1978. Predator activity in a rocky intertidal community. Relationship between predator foraging activity and environmental harshness. Oecologia (Berlin), Vol. 34, pp. l-16. MOORE, H. B., 1936. The biology of Purpura lapillus. I. Shell variation in relation to environment. J. Mar. Biol. Assoc. U.K., Vol. 21, pp. 61-89. MORGAN, P.R., 1972. The influence of prey availability on the distribution and predatory behaviour of Nucella lapillus (L.). J. Anim. Ecol., Vol. 41, pp. 257-274. MURDOCH,W.W., 1969. Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol. Monogr., Vol. 39, pp. 335-354. WOOD, L.H., 1968. Physiological and ecological aspects of prey selection by the marine gastropod Urosalpinx cinerea (Prosobranchia: Muricidae). Malacologia, Vol. 6, pp. 267-320.
J. Exp. Mar. Biol. Ecol., 1984, Vol. 79, pp. 91-103
Elsevier
JEM 290
BEHAVIOURAL
NUCELLA
COMPONENTS
LAPILLUS
OF PREY-SELECTION
BY DOGWHELKS,
(L.), FEEDING ON BARNACLES,
BALANOZDES
SEMIBALANUS
(L.), IN THE LABORATORY
S. DE B. DUNKIN
and R.N. HUGHES School of AnimalBiology, University College of North Wales, Bangor, Gwynedd, LL57 2UW. U.K. Abstract: Adult dogwhelks, maintained on mussels for 60 days before experimentation to reduce prior effects of ingestive conditioning and handling skills appropriate to barnacles, and thence deemed “inexperienced”, preferred the largest barnacles presented to them. Juvenile and adult dogwhelks, maintained on barnacles and deemed experienced, preferred barnacles of intermediate sizes that were correlated with the sizes of the dogwhelks. “Inexperienced” dogwhelks penetrated barnacles significantly more often by drilling than by prising, whereas experienced dogwhelks did the reverse. A predominant tendency to prise open barnacles was developed by previously “inexperienced” dogwhelks after they had eaten six to eight consecutive prey. Larger dogwhelks prised open greater proportions of larger barnacles than did smaller dogwhelks. Experienced adult dogwhelks prised open all barnacles of %2-mm opercular diameter but only 20% of those x6 mm in diameter. The preferred barnacles, 4-5 mm in opercular diameter, were of a size that the experienced adult dogwhelks could prise open in 50% of attacks. Dogwhelks inspected barnacles by crawling over them for % 20 min when the prey were subsequently rejected and w 30 min when subsequently eaten. Penetration time and ingestion time were linear functions of barnacle diameter, total handling time ranging from 4-26 h for barnacles of 2.5-2.7 mm opercular diameter. Experienced dogwhelks handled barnacles faster than “inexperienced” dogwhelks, largely because they used the quicker method of penetration by prising whenever possible. The yield of flesh per unit handling time was an accelerating function of barnacle size and, with experience, could be increased by a factor of x 1.2 for barnacles of 7 mm opercular diameter to x 2.0 for barnacles of 2 mm opercular diameter. The preference of experienced dogwhelks for barnacles somewhat smaller than the largest available, may have reflected the greater frequency with which these prey could be penetrated by the quicker method of prising. Minimizing handling time could be important in nature if there is a risk to feeding dogwhelks of being displaced by competitors. In the laboratory, 12% of dogwhelks where thus displaced. Barnacles of x 5 mm opercular diameter were estimated to be slightly more profitable than mussels of x 17.5mm shell length to a dogwhelk experienced with barnacles, but less profitable to a dogwhelk that has recently fed extensively on mussels. Dogwhelks, therefore, might switch between diets predominately of barnacles or of mussels if prey of comparable protitabilities change drastically in their relative abundance on the shore.
INTRODUCTION Nucella lapillus feed selectively when offered different sizes of one of their principal prey, Myzilus edulis (Bayne & Scullard, 1978 ; Hughes & Dunkin, 1984a). This selectivity is enhanced as dogwhelks gain experience with prey, but the preferred size of mussel is somewhat less than that predicted to yield the most flesh per unit handling time if 0022-0981/84/%03.00 0 1984 Elsevier Science Publishers B.V.
92
S.DEB.DUNKIN
AND R.N.HUGHES
feeding is unconstrained by extraneous factors (Hughes & Dunkin, 1984a). Barnacles are the other principal prey of I&W&J Iapitlu;s(Moore, 1936; Connelf, 1961; Largen, 1967; Morgan, 1972; Menge, 1978) and the present investigation quantifies the foraging behaviour of dogwheiks presented with barnacles in the faboratory, with particular reference to size-selection, yield per unit handling time and the effects on foraging of hunger, experience and interference from conspecific competitors.
MATERIAL
ANDMETHODS
Nucella lapillus (L.) of the sheltered-shore
morph (Hughes & Elner, 1979) were collected in April 1979 and irregularly thereafter from a stone jetty adjacent to Bangor pier (Ordn~ce survey reference SH 585733), where they had access to a dense popuiation of Sem~ba~an~s ~a~a~~~es (I,.) but not to ~ytilu~~ e&&s (L.) (Hughes & Dunkin, 1984a). Semibahus baianoides were collected, as required throughout the year, fixed to small stones from mid-tide level at Penmon, Anglesey (SH 625788). Experiments were conducted at 12 + 1 “C in a 12-h photoperiod. Aquaria contained recirculating sea water, maintained at 32-34x, S. EXPT. 1,SIZE-SELECTION
Barnacles were presented in abundances that approximately equalized the surface area represented by each size-class. Numbers used, obtained by scraping excess barnacles from the stones, were 26-34 barnacles of 2 to 3-mm opercular diameter (rostra-cane axis), 6-12 of? to 4-mm, 4-8 of 4 to 5-mm, and 3-6 of 5 to 6-mm. Stones bearing the barnacles, together with a dogwhefk, were placed in a 0.2 x 0.4-m aquarium and the dogwhelk allowed to feed for 7 days, after which the opercdar diameters of the eaten barnacles were measured. This procedure was repeated for 20 dogwhelks of 5 to IO-mm shell height, 20 of 15 to 20-mm, and 20 of 25 to 30-mm, representing first year, second year, and adult dogwhefks, respectively, ail of which had been mantled on a diet of barnacles for 60 days and then starved for I4 days to standardize hunger levels prior to experimentation. A further 20 adult dogwhelks, maintained for 60 days on mussels before starvation and therefore deemed “inexperienced” with barnacles, were subjected to the experimental procedure. Later experiments (Hughes & Dunkin, 1984b) showed that the effect of ingestive conditioning to barnacles would not have been eradicated completeIy after 60 days feeding on mussels, so that “inexperienced” can be used only as a relative term in the present context. Twenty aquaria containing the standard numbers of barnacles on stones, but lacking dogwhelks, served throughout the experiment to estimate the rno~~ty of barnacles not caused by predation,
NUCELLA EXPT.
2, METHODS
FEEDING
ON SEMIBALANUS
93
OF ATTACK
A stone bearing numerous barnacles of different sizes was placed together with a dogwhelk in a 0.2 x 0.4-m aquarium. The barnacles were inspected daily for 5 days noting the sizes consumed and whether the dogwhelk had gained entry by drilling through the opercular skeletal plates, drilling through the occludent margins of the opercular plates, or by prising the opercular plates apart. The experiment was repeated four times for each of 10 dogwhelks of 5 to lo-mm shell height, 10 of 15 to 20-mm, and 10 of 25 to 30-mm, and was run once for each of 40 “inexperienced” 25 to 30-mm dogwhelks. Experienced and “inexperienced” dogwhelks had been fed for 60 days on barnacles and mussels respectively, then starved for 14 days prior to experimentation. Four stones, densely covered with barnacles, were placed together with IO marked dogwhelks in a 0.5 x 0.35-m arena, over which was suspended a 16-mm Bolex camera, with synchronized flash, driven by a time-lapse mechanism giving exposures at 3-min intervals and loaded with a 30.5-m film lasting 7-g days. Durations of foraging behaviours were measured by counting frames with the aid of an L-W International Photo-Optical Data Analyzer. Prey-handling behaviour, as discernible on the film, was categorized into inspection time, defined as the time elapsing between the initial encounter of a dogwhelk with a barnacle and either rejection of the prey or initiation of attack, and post-inspection handling time, defined as the time elapsing between initiation of attack and abandonment of the prey. Initiation of attack was recognized as the cessation of exploratory movements of the dogwhelk over the barnacles for 1 h, determined from the analysis of previous frames. Completion of penetration and commencement ofingestion could not be distinguished on the film. Ingestion time was, therefore, measured directly from dogwhelks consuming barnacles whose opercular plates had been removed before presentation (Expt. 4). Penetration time was estimated as the difference between predicted post-inspection handling time and ingestion time. Dogwhelks handling barnacles were sometimes invaded by competitors and the ensuing interactions were timed from the film. EXPT.
3, EFFECT
OF HUNGER
ON HANDLING
BEHAVIOUR
Barnacles presented were of 4 to 6-mm opercular diameter, other sizes having been scraped off the stones. Four batches of 10 adult dogwhelks were starved for 0, 14,30, and 90 days prior to experimentation. Five dogwhelks from each of two starvation regimes were introduced into the arena and filmed. Four films were taken, covering all 40 experimental dogwhelks. Inspection time, post-inspection handling time and competitive interactions were measured from the films. EXPT.
4, EFFECT
OF EXPERIENCE
ON HANDLING
BEHAVIOUR
The natural covering of barnacles on the stones was used, incorporating barnacles of 2.0 to 7.5~mm opercular diameter. The opercular plates of ~40 barnacles were prised
94
S. DE B. DUNKIN
AND R.N. HUGHES
apart to allow dogwhelks immediate access to the flesh, so that ingestion time could be measured. Dogwhelks deemed experienced had been maintained solely on barnacles for 60 days and then starved for 14 days to standardize hunger levels prior to experimentation. Dogwhelks deemed “inexperienced ” (see Expt. 1 above) had been maintained solely on mussels for 60 days before starvation. Five experienced and five “inexperienced” dogwhelks were introduced into the arena and filmed. Eight films, covering 40 experienced and 40 “inexperienced” dogwhelks, were taken. Inspection time, post-inspection handling time, ingestion time, and competitive interactions were measured from the films. Penetration time was estimated from the predicted postinspection handling time and ingestion time. YIELD
OF FLESH FROM A BARNACLE
Dogwhelks consumed all the flesh of each barnacle attacked. The flesh of different sized barnacles was dissected from the exoskeleton, dried at 70 “C for 72 h and weighed. Barnacle dry flesh weight was related to opercular diameter by regression analysis. RESULTS EXPT.
I, SIZE-SELECTION
The size-frequencies of dead barnacles in the experimental aquaria were significantly different from those in the control aquaria (Fig. la,b, Log Likelihood Ratio, G = 162.7, d.f. = 3, P < 0.001) and the numbers of undrilled dead barnacles were significantly greater in the control aquaria (G = 36.2, d.f. = I, P < 0.001). Successively larger experienced dogwhelks preferred successively larger barnacles (Fig. Ic-e), although only the means for the smallest and largest dogwhelks were significantly different by Mann-Whitney U-test (Fig. 1, legend). The mean size of barnacles eaten by “inexperienced” dogwhelks was significantly larger than that for experienced ones (Fig. le,f). EXPI‘. 2. METHODS
OF ATTACK
“Inexperienced” dogwhelks penetrated barnacles significantly more often by drilling than by prising, whereas experienced dogwhelks did the reverse (Table I), Previously “inexperienced” dogwhelks developed a predominant tendency to prise open barnacles after six to eight consecutive prey had~been eaten (Fig. 2). The proportion of barnacles prised open depended upon the relative sizes of the predator and prey, larger dogwhelks prising open higher proportions of larger barnacles than did smaher dogwhelks (Fig. 3). EXP’I.
3, EFFECT OF HUNGER
ON HANDLING
BEHAVIOIJK
Hunger had no significant effect on inspection time (ANOVA, F = 1.OO,d.f. = 3.40, P > 0.35) or on post-inspection handling time (F= 1.53, d.f. = 3.34, P > 0.2).
NUCELLA
95
FEEDING ON ~~~IBALA~US
d 5 -IO
dogwhelks X-30
mm
degwhetks IS-20 mm
f r dogwhelks
mm
25-30 nm
~ 2
4
6 Opercutar
2 diameter
[mm]
4
I 6
Fig. 1. a, size-specific mortality rates of barnacles in the control aquaria; b, size-specific mortality rates of barnacles in aquaria containing dogwhelks of 25 to 30”mm shell height; c, d, e, size-frequencies of barnacles eaten by experienced dogwhelks; f, size-frequencies of barnacles eaten by “inexperienced” dogwhelks; histograms c-f each represent 20 barnacles consumed by 20 dogwhelks; Mann-Whitney U-tests of raw data for differences between mean sizes ofbarnacles eaten were: c with d, U = 145.5, P > 0.05; d with e, U = 148, P > 0.05; c with e, U = 95, P < 0.05; e with f, U = 114, P < 0.05.
S. DE B. DUNKJN AND R.N. HUGHES
96
Numbers of barnacles prised or drilled by adult dogwhelks that bad prcv~ously been fed on barnacles (experienced)or mussels (“inexperienced”) for 60 days before the feeding trials: Fisher exact probability test, P c a.001
_,
. . _...~._. -.
Experienced
**Inexpe~ence~
. Prised
26
?
Drilled
2u
R?
0
2
4
No. consecutive
6
8
-_
10
prey eaten
of
Kg. 2. The percentage of attacks made by 20 previously naive dogwhelks, involving drilling the skeletal plates (----), drilling of the opercular occludent margins (, . . .), prising of the opercular plates (). plotted against the cumulative number of barnacles eaten per dogwheIk.
91
FEEDING ON SEMIBALANUS
NUCELLA
a
100
l--l
dogwhelks S-10
mm
60
100
“r
25-30 mm
t 60 i
20
3.0 Opercular
50
k0 diameter
[mm
60
I
Fig. 3. The frequencies with which barnacles in successive size-categories were prised open by experienced dogwhelks (a, b, c) and “inexperienced” dogwhelks (d): each histogram represents 40 barnacles.
EXPT. 4, EFFECT OF EXPERIENCE
ON HANDLING
BEHAVIOUR
Inspection time was significantly longer prior to the attack (29 +_2 min (SE)) than to the rejection (19.8 + 2 min (SE)) of a barnacle (F = 37.78, d.f. = 1,282, P < O.OOl),but was not significantly correlated with barnacle size (F = 0.56, d.f. = 4, 282, P > 0.65). Experience had no significant effect on inspection time either prior to the attack (F = 0.78, d.f. = 9, 124, P > 0.35) or to the rejection of a barnacle (F = 0.33, d.f. = 1, 122, P > 0.55). Inspection time was significantly shorter in the presence of competitors
98
S. DE B. DUNKIN AND R.N. HUGHES
prior to the attack (21 & 2 min (SE), F = 10.11, d.f. = 1, 159, P < 0.01) but not prior to the rejection of a barnacle (F = 2.03, d.f. = 1, 122, P > 0.5s). Post-inspection handling time was correlated with barnacle opercular diameter and was significantly longer for “inexperienced” than for experienced dogwhelks (Fig. 4). 0 0
0
0
O
0
.
0
16
l cl
0
.
0
12
8
4
0 2
3
4 Opercular
5 diameter
6
7
[m ml
Fig. 4. The time taken for adult dogwhelks to penetrate and ingest barnacles, plotted against size of the prey: 0, experienced dogwhelks; 0, “inexperienced” dogwhelks; the lines were derived from regression equations fitted to the data (see text).
Regression equations (2 SE) fitted to the data were: “inexperienced” dogwhelks, y = (1.08 + 0.09) x + (5.17 + O.l6), n = 53, PC 0.001, experienced dogwhelks, y = (1.59 F 0.11) x + (4.01 +_O.lS), n = 65, PC 0.001,where y = log, (postinspection handling time, min) and x = log, (barnacle opercular diameter, mm). The slopes of the regressions were Significantly different (I= 2.60, d.f. = i 15, P -=z 0.02).
Ingestion time was correlated with bamacle 0~~~~~ diameter (Fig. 5) but there was no si~c~t ~~~en~e between the slopes (t = 1.89, d.f. = 25, P > 0.05) ortheintercepts (t = 2.04, d.f. = 25, P > 0.05) of regressions for experienced and ‘~inexpe~enc~~’ dogwhelks. Pooled data were fitted by the regression: y = (162.1 + 19.5) 1, where y = ingestion time (min) and x - (124.4 + 10lS), n = 29, P -K0.00 x = barnacle operctiar diameter (mm).
01 2
L
t
L
Opercular
1
8
6 1mm f
I
diameter
Fig. 5. Time taken for adult do~helks
to ingest the flesh of barnacles whose opercular plates had been prised open before presentation, plotted against size of the prey: 0, experienced do~helks; 0, ~inex~~enced~ do~helks; the line represents the regression equation fitted to the pooled data (see text). 12 .
a 0 0 0
ru ? .r_ E
0
0 .
8
0 0
2
3
0
a 00
o”
L
5
6
0
7
8
Oparcuiot diameter In& Fig. 6. Time taken by adult do~helks to penetrate barnacfes by drilhng (0) or prising (a), plotted against size of the prey: the lines represent regression equations fitted to the data (see text).
l(W)
S. DE B. DUNKIN AND R.N. HUGHES
Penetration time was an approximately Iinear function of bamacie opercular diameter over the range of prey sizes used and was significantly longer when penetration was by drilling than by prising (Fig. 6). Regressions fitted to the data were: drilhng: v = (64.7 + 15.2) x - (75.9 + 92.11, n = 78, P < 0.005, prising: f: = (47.7 * 12.3) X - (106.8 + 62.5), n = 40, P < 0.00’7, where y = penetration time (min) and .X= barnacle opercular diameter (mm). The slopes of the regressions were significantly different fb = 2.32, d.f. = 114, P < 0.02).
2
3 Opercular
4
s
6
diameter Imml
Fig. 7. The time eiapsing between the arrival of an intruding dogwhelk at a barnacte already being handled by another dogwhelk and the departure of one of the dogwhetks, ptotted against size of the prey.
12 y0 of feeding dogwhelks were displaced by competitors. The duration of competitive encounters between intruding dogwhefks and the original occupants of barnacles was negatively correlated with barnacle size (Fig. 7) and was described by the regression equation: y = ( - 1.88 + 0.77) x I- (30.19 + 4.33), n = 26, P - 0.01, where y = encounter duration (min) and x = barnacle opercuiar diameter (mm).
101 YIELD OF FLESH FROM A BARNACLE
Barnacle dry flesh weight was related to opercular diameter by the regression equation: y = (3.61 2 0.34) x - (4.06 k 0.47), n = 52, P < 0.001, where y = log, (dry flesh weight, mg) and x = log, (opercular diameter, mm).
DISCUSSION
Dogwhelks previously maintained on mussels and assumed to have lost some of the effect of ingestive conditioning (Wood, 1968) or of temporarily developed handling skills (Hughes & Dunkin, 1984a) for barnacles, preferred the largest barnacles offered. Preference for the largest barnacles available has also been recorded in dogwhelks freshly collected from a shore where they had already been feeding predominantly on barnacles (Barnett, 1979). The West North American species, Thais lumellosa and T. canuliculutu, have been reported to prefer the larger barnacles among those available (Connell, 1970; Dayton, 1971), although Semibalunus curiosus may reach a threshold size at which it becomes less attractive or even immune, to dogwhelks (Dayton, 197 1). In the present investigations, however, dogwhelks that had gained experience feeding on barnacles shifted their preference to prey somewhat smaller than the largest available. This behaviour is not predictable from the potential profitability of the prey (yield of flesh/total handling time), which is an increasing function of barnacle size (Fig. 8). Time taken for prising is about 0.53 times that for drilling barnacles of 2-mm opercular diameter and about 0.64 times that for drilling 6-mm barnacles (regressions, Expt, 4). By changing from drilling to prising, dogwhelks increase the profitability of prey (Fig. 8) by a factor of sz 1.2 for barnacles of 7-mm opercular diameter to z 2.0 for 16-
‘; .:
12-
28
0'
0
1
I
I
I
2
L
6
8
Opercular
diameter
[ mm 1
Fig. 8. Profitability of barnacles to adult (25-30 mm) dogwhelks, calculated as (dry weight of ingested flesh)/(inspection + penetration + ingestion time) using regression equations given in the text, plotted against prey size for experienced (upper curve) and “inexperienced” (lower curve) dogwhelks.
102
S. DE B. DUNKIN
AND R.N. HUGHES
barnacles of 2.5mm. Larger barnacles, however, become harder to prise open, the proportion prised by experienced dogwhelks falling from 100% for barnacles of 2-mm opercular diameter to x 20 7; for those of 6-mm (Fig. 3). Dogwhelks preferred sizes of barnacles that they could prise open with z 50% chance of success. But even allowing for the lower probability that larger barnacles will yield to prising, their average profitability is still greater than that of smaller barnacles. Emlen (1966, discussed in Hughes, 1980) found that Thais emurginata preferred barnacles smaller than the largest available and demonstrated that the profitability of the largest Semibalanus cariosus could be devalued by x 307; when competing dogwhelks interfered with the handling of prey and stole flesh. Consequently, the average protitability of the largest was less than that of smaller S. cariosus, perhaps explaining the size-selection by Thais emarginata. In .the present study, Nucella lapillus were displaced by “interlopers” in 12% of cases while handling Semibalanus balanaides, compared with 61 y0 while feeding on Mytilus edulis (Hughes & Dunkin, 1984), probably reflecting the difference in prey size. “Interlopers” are able to steai flesh by gaining entry through the gaping valves of a mussel that has already been drilled (Hughes & Dunkin, 1984a). Similarly, in the case of large Semibalanus cariosus, there is room for several interloping Thais emarginata to drill and steal flesh from the original occupant (Emlen, 1966). Semibalanus balanoides, however, is too small for more than one dogwhelk to handle simultaneously, with the result that interlopers could devalue the prey item only by prolonging handling time or by displacing the original occupant. Interlopers did not significantly lengthen handling time (Expt. 4). Displacement by an interloper, on the other hand, could be seriously disadvantageous if it occurred long after the original occupant had begun its attack on the barnacle. Inspection and penetration time together ranged from z 45 % of total handling time for barnacles of 2-mm opercular diameter to x 30 % for those of 6-mm opercular diameter (regressions, Expt. 4). Connell (1970) estimated that Thais larnellosa spent NN 70-80% of total handling time penetrating Semibalanus curiosus. There is, therefore, a chance that dogwhelks may be displaced even before any flesh has been ingested. Total handling time for Nucella lapillusfeeding on Semibalanus balanoides ranged from 4-26 h (regressions, Expt. 4) and was estimated to be x 2 1.7 h from the data of Connell (196 l), leaving little time during high tide, when dogwhelks are active (Connell, 1961, 1970) for a displaced dogwhelk to attack another barnacle. A tidal constraint on foraging time, together with risks from competitors, could devalue the average profitability of larger barnacles estimated on the assumption of unhmited foraging time. We can offer no explanation for the size-selection other than being a means of maximizing the yield of flesh within the constraints imposed by the risk of competition in a limited foraging period, or a means of minimizing the time spent foraging, during which a dogwhelk could be at risk to predation, dislodgement by waves or desiccation.
NUCELLA
FEEDING ON SEMIBALANUS
103
ACKNOWLEDGEMENT
We gratefully acknowledge the support of NERC grant GR3/3695.
REFERENCES BARNE’IT,B.E., 1979. A laboratory study of predation by the dogwhelk Nucella lapillus on the barnacles Elminius modestus and Balanus balanoides. .l. Mar. Biol. Assoc. U.K., Vol. 59, pp. 299-306. BAYNE,B. L. & C. SCULLARD,1978. Rates of feeding by Thais (Nucella) lapillus(L.). J. Exp. Mar. Biol. Ecol., Vol. 32, pp. 113-129. CONNELL,J.H., 1961. Effects of competition, predation by Thais lapillus and other factors on natural populations of the barnacle Balanus balanoides. Ecology, Vol. 42, pp. 710-723. CONNELL,J. H., 1970. A predator-prey system in the marine intertidal region. I. Balanus glandula and several predatory species of Thais. Ecol. Monogr., Vol. 40, pp. 49-78. DAYTON,P. K., 1971. Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr., Vol. 41, pp. 351-389. EMLEN,J.M., 1966. Time, energy and risk in two species of carnivorous gastropod% Ph.D. dissertation, University of Washington, Seattle, 112 pp. HUGHES, R.N., 1980. Optimal foraging theory in the marine context. Oceanogr. Mar. Biol. Annu. Rev., Vol. 18, pp. 423-481. HUGHES, R.N. & S. DE B. DUNKIN, 1984a. Behavioural components of prey selection by dogwhelks, Nucella lapillus(L.), feeding on mussels+Uytilus edulis L., in the laboratory. J. Exp. Mar. Biol. Ecol., Vol. 77, pp. 45-68. HUGHES, R.N. & S. DE B. DUNKIN, 1984b. Effect of dietary history on selection of prey, and foraging behaviour among patches of prey, by the dogwhelk, Nucella lapillus (L.). J. Exp. Mar. Biol. Ecol., Vol. 79, pp. 159-172. HUGHES, R.N. & R. W. ELNER,1979. Tactics of a predator, Carcinus maenas, and morphological responses of the prey, Nucella lapillus. J. Anim. Ecol., Vol. 48, pp. 65-78. LARGEN,M. J., 1967. The diet of the dog-whelk, Nucella lapilh (Gastropoda : Prosobranchia). J. Zool., Vol. 151, pp. 123-127. MENGE, B.A., 1978. Predator activity in a rocky intertidal community. Relationship between predator foraging activity and environmental harshness. Oecologia (Berlin), Vol. 34, pp. l-16. MOORE, H. B., 1936. The biology of Purpura lapillus. I. Shell variation in relation to environment. J. Mar. Biol. Assoc. U.K., Vol. 21, pp. 61-89. MORGAN, P.R., 1972. The influence of prey availability on the distribution and predatory behaviour of Nucella lapillus (L.). J. Anim. Ecol., Vol. 41, pp. 257-274. MURDOCH,W.W., 1969. Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol. Monogr., Vol. 39, pp. 335-354. WOOD, L.H., 1968. Physiological and ecological aspects of prey selection by the marine gastropod Urosalpinx cinerea (Prosobranchia: Muricidae). Malacologia, Vol. 6, pp. 267-320.