Download Interindividual Variation in Prey Selection by the Snail Nucella

Interindividual Variation in Prey Selection by the Snail Nucella (= Thais) Emarginata
Author(s): Lani West
Source: Ecology, Vol. 67, No. 3 (Jun., 1986), pp. 798-809
Published by: Ecological Society of America
Stable URL: http://www.jstor.org/stable/1937702
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Ecology, 67(3), 1986, pp. 798-809
? 1986 by the Ecological Society of America
INTERINDIVIDUAL VARIATION IN PREY SELECTION
BY THE SNAIL NUCELLA (= THAIS) EMARGINATA'
LANI WEST
HopkinsMarine Station of Stanford University,PacificGrove,California93950 USA
Abstract. Variation in diet among individuals of a population of carnivorous marine snails in a
rocky intertidal environment of central California was analyzed. Nucella emarginata drills and eats
barnacles, mussels, and limpets. Out of 128 marked snails, 104 were observed through two or more
feeding attacks in the field during the 4-mo study. Fifty-one of these snails were observed through
five or more sequential feeding attacks. Three major points are illustrated. (1) Within each study site,
individuals close to the same size often chose strikingly different diets. (2) There was a range of dietary
specialization and generalization among individuals foraging in the same habitat. Individuals showed
a high degree of consistency in their diets. While the population of N. emarginata attacked seven prey
species at site A and four prey species at site B, no individual snail observed in this study ate more
than three species of prey. (3) Food choices made by each individual were not a simple reflection of
the relative abundance of the surrounding prey species or the differences in microhabitat prey distribution that each predator encountered. These conclusions remained the same for several different
methods of measuring prey availability. I suggest that Nucella emarginata diet patterns have a variety
of causes, which may include ingestive conditioning, learning, and genetic variability.
Key words: conditioning;feeding experience;foraging;intertidalzone; intrapopulationvariability;
learning;Nucella emarginata;predator-preyinteractions;prey selection;variationin diets.
INTRODUCTION
Although individual differences between members
of the same population have long been recognized,
most ecologists exploring the interactions of populations evaluate pooled data on large numbers of organisms. Traditionally, niche theory (Hutchinson 1959,
MacArthur 1968), studies of community structure and
dynamics (Whittaker 1965, Connell 1975, Menge and
Sutherland 1976), and optimal foraging theory (Emlen
1966, Pyke 1984) have not dealt with variability among
individuals in a population or habitat. On the other
hand, some ecologists (see Heinrich 1976, 1979, Werner et al. 1981) study population characteristics and
interactions by noting variability between individual
population members, since changes within populations
are due to selection acting on interindividual differences.
Intrapopulation variation has been considered by
geneticists (Dobzhansky et al. 1977, Wright 1978,
Coulthart et al. 1984), behaviorists (Krebs 1970, Curio
1976), and population biologists interested in resource
use (Hassell and Southwood 1978, Tabashnik et al.
1981, Jaenike and Grimaldi 1983). Van Valen (1965)
explored morphological variation in bird populations
and proposed that birds living in patchy environments
will show interindividual variation in feeding activities
and associated morphology. Grant (1971) in his studies
of bird tarsae, expanded this idea by pointing out that
a population can be made up of members that "differ
in their modes of exploitation, being either specialists
or generalists" or "individuals that are similar (pro1 Manuscriptreceived 9 October 1984; revised 16 March
1985; accepted 1 April 1985.
vided variances are small) and are all generalists."
Roughgarden (1972, 1979) treated some of these ideas
theoretically when modeling components of niche
width. He suggests that a population's degree of interindividual specialization is dependent on competition
and on productivity in the population's surroundings.
As yet there are not enough empirical studies of interindividual variability to evaluate these ideas. The only
way to distinguish between a population of generalists
and a population of specialists arrayed along a resource
spectrum is to examine individuals.
Studies of individuals are also relevant to optimal
foraging theory (Krebs 1978, Hughes 1980, Pyke 1984).
Foraging behavior is usually viewed from the perspective of the average individual of the population or
species, but knowledge of interindividual variability
may be essential for the construction of realistic foraging models. Hughes (1979) incorporated recognition
times, probability of prey misidentification, and learning into a traditional optimal foraging model, and predicted that when a predator learns to handle certain
prey more efficiently, that prey's position in the predator's preference hierarchy may change. Prey recognition, handling, and other aspects of foraging that involve learning are traits that can be influenced by genetic
characteristics of the individual and the microhabitat
the predator lives in. Thus these traits are likely to vary
among individuals.
The goal of this study was to examine in detail the
feeding behavior of individuals in a population of marine snails. The study animal, Nucella (=Thais) emarginata, is a rocky intertidal carnivore that feeds on a
variety of barnacles, mussels, and limpets. This snail
and other members of its genus have been shown to
PREY SELECTION BY INDIVIDUAL SNAILS
June 1986
TABLE
799
1. Densities of carnivorous snails summarized from daily (98 d) counts of individuals on the study surfaces at low
tide.
Snail density (no./M2)
Site B*
Site A*
Species
Mean
Range
SD
Mean
6.71
1.36
1.21-5.32
4.55
Nucella emarginata
0.88
0.47
0-0.78
0.67
Acanthina punctulata
0
0.52
0-0.50
0.55
Acanthina spirata
0.26
0
Ocenebra circumtexta
* Total surface area of study sites is 14. 10 m2 for site A and 18.13 m2 for site B.
be important predators in rocky coastal areas of Great
Britain (Connell 1961, Morgan 1972), New England
(Menge 1978a, b) and the northeast Pacific (Connell
1970, Dayton 1971, Spight 1974, Palmer 1983).
The present study (1) documents foods selected by
marked individual predators surrounded by the same
array of prey species, (2) analyzes the degree of consistency within individuals' diets over time, and (3)
examines the relationship between the diet of an individual snail and the relative availability of its prey,
using a variety of methods to measure prey availability.
The results indicate that individual snails are choosing
different diets from the same array of prey species in
their natural environment. Furthermore, the choices
made by each individual do not simply reflect the relative abundance of the surrounding prey species or
differences in prey distribution within the microhabitats that the predator encounters. This study was not
a test of optimal foraging theory. However, as discussed
above, its results are relevant to the assumptions made
by that theory in its simplest forms.
STUDY SITES AND BIOTA
This study was carried out in Pacific Grove, California (36?36' N, 121l54' W). Study sites were the eastern shore of Mussel Point (site A), and rocks adjacent
to Point Alones (site B), both of which are on the
property of Hopkins Marine Station of Stanford University. Study sites were examined during each period
of lower low water between 26 January and 18 May
1978. The study sites are inhabited by Nucella emarginata and three other species of carnivorous snails
(Table 1). Of those species, Nucella emarginata occurred in the highest densities at both study sites. Prey
species eaten at the two sites were the barnacles
Chthamalus spp., Balanus glandula, and Tetraclita rubescens, and the limpets Collisella scabra and C. rimatula. Two species of prey found at site A, the barnacle
Pollicipes polymerus and the mussel Mytilus californianus, were absent at site B. Common sessile or slowmoving animals that occur at both sites but were not
eaten by Nucella emarginata were the gastropods Littorina scutulata, Tegula funebralis, Littorina planaxis,
and Collisella digitalis; the chiton Mopalia muscosa;
the tube-dwelling polychaetes Dodecaceriafewkesi and
Range
SD
0.39-9.21
0.06-2.59
2.64
0.78
0-0.83
0.27
Phragmatopoma californica; and the sea anemone Anthopleura elegantissima. All study site surfaces were in
the upper part of the middle intertidal zone in a region
of protected outer coast (Ricketts and Calvin 1968).
Site A consists of an irregular projection of granitic
rock, surrounded by sand and directly in the path of
incoming waves. Site B is less exposed, shielded from
direct surf by offshore rocks, and is characterized by
tightly wedged granitic boulders. In addition to the
animals listed above and in Table 1, the erect algae
Endocladia muricata and Gigartina papillata, the encrusting red alga Hildenbrandia occidentalis, and a film
of microscopic red and green algae are common at both
sites. A more detailed description of the intertidal areas
surrounding Hopkins Marine Station can be found in
Glynn (1965). Information on the natural history of
Nucella emarginata is supplied in Abbott and Haderlie
(1980).
METHODS
Activity and the process of predation by N. emarginata were observed in the field. After selecting its
prey, Nucella normally drills through the shell, inserts
its proboscis, and rasps out the soft body parts with
the radula. Observations made at both low and high
tides indicate that the snails are most active when submerged; they remain relatively inactive after exposure
to air at low tide. If an animal is feeding at the time
of a receding tide, it continues to grip its prey while
exposed to air. The predator's proboscis is usually not
extended into the prey during low tide, but the snail
remains in the feeding position until it is submerged
again. Snails remained with the same individual prey
from hours to days, depending on the size and species
of the prey. Approximate feeding times presented in
this paper (Table 2) were determined by field observation once per day. The subject of biases due to different handling times of prey and daily observation
techniques will be discussed below (see Results).
Every effort was made to observe the snails and their
prey with minimal disturbance. When it was necessary
to tilt a snail gently away from the substrate to detect
prey, snails rarely lost their foothold or moved away.
Where activities were difficult to observe, a small hand
mirror was used to view beneath the animal or inside
TABLE
Ecology, Vol. 67, No. 3
LANI WEST
800
2.
Sizes and consumption times of prey species eaten by Nucella emarginataon the study site surfaces.
Site A
Time (d)
Prey size (mm)
Species
Chthamalusspp. basal diameter
Balanusglandulabasal diameter
Pollicipespolymerusrostrum-carina length
Tetraclitarubescensbasal diameter
Collisellascabrashell length
Collisellalimatula shell length
Mytiluscalifornianusshell length
X
SD
Range
N*
X
SD
2.90
3.80
9.95
17.75
7.80
8.50
17.43
0.68
1.91
5.19
6.51
2.50
3.12
10.00
2.0-5.0
2.5-9.0
4.0-16.5
10.0-24.0
5.0-10.5
6.0-12.0
5.0-33.5
26
124
50
12
24
3
56
1
1.12
1.41
1.33
1
1.05
3.32
0
0.399
0.874
0.577
0
0.242
3.99
Ranget
<1-1
<1-3
<1-4
<1-3
<1-1
<1-2
<1-8
* Numbers of prey eaten (N) include observations from unmarked snails that fed within the study site.
t Range values preceded by the symbol < indicate that some snails finished eating within one tide cycle.
crevices. When an individual snail was found clinging
to potential prey, the presence of a partially or completely drilled bore hole through the shell of the prey
was considered indicative of active predation. Sometimes prey were consumed without showing evidence
of boring marks. These occasions were infrequent, but
the act of predation was substantiated by observation
of partially digested prey tissue and/or the characteristic way N. emarginata grip their prey (encircling the
prey individual with the anterior portion of the foot
and locating the buccal mass on top of the opercular
plates of a barnacle or between the valves of a mussel).
The movements and feeding activities of individually marked snails were followed to obtain a record
of their diets in relation to food availability. Since N.
emarginata ranged through the upper middle intertidal
zone, it was possible to make daily observations, missing only those lower low water periods when the surf
was exceptionally high (N = 6 out of a total of 104
observation periods).
Study sites were carefully mapped to scale to show
topography and locations of sessile species. Within each
site, N. emarginata were individually marked in place.
Quick-setting epoxy was used to glue numbered canvas
tags (W. H. Brady Company, Milwaukee, Wisconsin,
Wire Marker Tags) to the snail shell. At times when a
simpler (but short-term) marking technique was necessary, colored wax crayons provided satisfactory identification of individuals. Shell length of all marked snails
(from apex to siphonal canal tip) was measured with
vernier calipers to the nearest 0.5 mm. Snails were
measured at the beginning and end of the study, but
only beginning sizes are reported in this paper because
maximum growth in shell length was <2 mm. The
position of the snail, its feeding activity, the nature and
size of its food (if any), and the prevailing environmental conditions (time, degree of sunlight, rain or fog,
general surf conditions) were recorded on photocopied
maps of the study site.
The precise location of each marked snail was determined at each observation by measuring its position
with respect to two established landmarks on the study
surface. Snail movement paths were estimated by con-
nesting successively mapped positions of an individual
with straight lines that followed the major contours of
the substrate surface.
The measurement of prey availability
In prey selection studies in nature it is important to
compare the diet of an individual predator to the relative availability (accessibility) of the various prey
species surrounding it. However, it is difficult to define
and to measure the specific factors that determine the
accessibility of the prey item to that predator. An ideal
measure of availability, based on the actual number of
potential prey of each species encountered by a predator before feeding occurred, would require continuous
monitoring of the movements of the predator. This
was not feasible. Two alternative methods of measuring availability are described below. Only prey individuals within the size range of prey observed to be
eaten during the study were counted (Table 2).
First, estimates were made of the percentage of the
rock surface covered by potential prey species of Nucella emarginata, either on the whole rock surface or
some subdivision of that surface. Percentage cover of
each prey species was determined from photographic
slides taken at 2-wk intervals throughout the study.
Each slide portrays a square metre of study site surface.
These photographic slides were viewed under a dissection microscope to resolve species >2 mm in size.
One hundred random points were superimposed on
each slide. All points falling on potential prey, on open
rock, crustose algae, diatoms or on prey smaller than
the size range observed to be eaten were tabulated.
Second, estimates were made of the number of potential prey of each prey species present either on the
whole rock surface or on some selected subdivision of
that surface. These measures were made in two ways.
(1) Ten randomly positioned, 100-cm2 quadrats were
placed over each approximate square metre of study
site surface. At site A, 14 m2 were monitored; at site
B, 18 M2. All potential prey individuals were counted
within the quadrats in the field. From these data I
estimated densities of each prey species. These measures were made once, 2 mo after the study began, and
Site B
Time (d)
Prey size (mm)
X
SD
3.20
5.53
0.72
2.08
. . .
4.12
4.50
.
801
PREY SELECTION BY INDIVIDUAL SNAILS
June 1986
Range
N*
X
SD
Ranget
3.0-6.5
2.0-12.0
13
269
1
1.09
0
0.324
< 1-1
< 1-4
. . .
.
4.0-20.5
2.0-8.0
0.83
3.12
. . .
. . .
. . .
1.37
1
0.807
0.008
< 1-4
< 1-2
. . .
51
4
same length as the observed diet sequence were calculated. Those probabilities that were less than or equal
to that of the observed diet studied were added to the
probability of the observed diet. This calculation yields
the probability of obtaining the observed diet and all
possible diets equally or more specialized, taking into
account the availability of the prey species. These probability values are conservative because they account
only for the number of prey species in the diet, not the
order in which those prey species occur.
RESULTS
do not take into account seasonal changes in availability. (2) Transect lines (2 cm wide, the approximate
width of a snail's foot), along the estimated snail movement paths described above were superimposed on a
photograph of that area. The photograph was taken
within a week of the time of feeding observations.
Counts of individuals of each prey species were then
made from the photograph.
Counts of the two barnacle species Chthamalus dalli
and Chthamalusfissus were combined as Chthamalus
spp., because it is difficult to distinguish these two
species without dissecting the animal. In all counts
from photographic slides I combined Balanus glandula
and Chthamalus spp. into one group because they frequently could not be distinguished in the photographs.
Limpets were the only mobile prey eaten in the study.
Collisella scabra individuals each have a specific home
site on the rock, and photographs repeated at 2-wk
intervals seldom showed differences in their low tide
positions. Collisella limatula, on the other hand, does
not home; however, individuals were usually near their
previous positions.
Probability calculations
The probability of a given snail eating the observed
diet, assuming that it ate prey species according to their
relative abundance, was calculated by computer using
the multinomial distribution (Feller 1968).
ki!k2!
...
kr! PIP2P
3
. . .
Pr
where:
n represents the total number of observed feeding attacks made by one snail.
kid'sare the number of times the snail fed on prey
species i.
pi(i = 1, . . , r) represents the relative abundance of
i, where PI+ . . . + Pr = 1. I used the
density values for i (see The Measurement of Prey
Availability) instead of the percentage cover values,
because they were larger and more conservative when
used in this test.
For each observed diet the probabilities of all the
other possible combinations of prey in sequences the
prey species
The data suggest that prey selection by the N. emarginata population does not simply reflect the relative
abundance of those prey species in the environment
(Fig. 1). Seven prey species (barnacles, limpets, and
mussels) were eaten at site A; four prey species (barnacles and limpets) were eaten at site B (Fig. 1). Balanus, Pollicipes, Mytilus, and Tetraclita were actively
selected from among other prey species available in
the habitat. Collisella species were taken either in proportion to their abundance or taken in smaller numbers
than would be suggested by their abundance. Chthamalus species were always taken in low numbers compared to their abundance in the environment.
Different attack techniques were used for each prey
species eaten. The barnacles Balanus, Chthamalus, and
Tetraclita were drilled between the paired tergal plates
or between the paired scutal plates. None ofthese species
of barnacles were ever observed to be drilled at the
location between a tergal and scutal plate. Similarly,
Palmer (1982) found more northern N. emarginata to
drill through the opercular plates of B. glandula and
Semibalanus cariosus. In my study it appeared that the
snail "prised" open the plates without drilling in a few
cases, as reported by Dunkin and Hughes (1984) for
N. /apillus feeding on Semibalanus balanoides. In contrast, the remaining species of barnacle, Pollicipes, was
drilled laterally between the rostral and scutal plates
in every attack. Nucella ate the limpets Collisella scabra and C. /imatula without drilling or drilled at the
margin of the shell to form a small nick, extending the
proboscis under the shell margin, or sometimes flipping
the limpet to expose the foot. Though N. emarginata
show drill site specificity on most prey, Mytilus californianus eaten by N. emarginata were not examined
for drill site specificity because the snails could rarely
attain surface access to all parts of the mussel shell.
Mytilus californianus commonly occur in dense clumps
with members of their own species and mixed with
Pollicipes. Mussels were also sometimes embedded in
the surrounding tubes of the polychaete Phragmatopoma. Thus accessibility of the mussel surface to the
snail will bias the patterns in drill site position on
mussels.
The population of N. emarginata is relatively generalized in overall diet but consists of individuals with
varying degrees of specialization. Out of 128 marked
Ecology, Vol. 67, No. 3
LANI WEST
802
RELATIVE ABUNDANCE
OF PREY
RANDOM
SITE A
ChthOmo/us spp.
Ba/onus q/ondu/o
Col//se//a scabrG
Pol//cipes polymers
Co/I/se//o limotulo
Myti/us ca//fornianus
Tetrac/l/a rubescens
2
2
I
SITE B
100
Chthamo/us
spp.
Ba/onus
q/andu/a
58
Tetroc/ifa
rubescens
scatra
Co/I/se//a //ma1u/a
OTHER SPECIES
SPECIES SMALLERTHAN EATEN
ROCK/CRUSTOSE ALGAE/DIATOMS
8
17
.
19
4
r---
'0
OF FEEDING ATTACKS
9
3
AKDSAL
UNMARKED
0 0
50
,
32
a
1
I
100
142
6
6
1
3
I
24
gNUMBER
9
13
ALGAE/DIATOMS
OF PREY
CHANGED TO %
0 0
50
8
10
6
OTHERSPECIES
24ALLERTHANEAT?N
SPECIES SMALLER
THAN EATEN
Cal//se//a
DIET
NUMBERS
NUMERICALCOUNT %=
100
50
7;1
OTHERSPECIES
ROCK/CRUSTOSE
E
POINT%
51
59
50
.
-
5
100
.
4
80
._
15
9
7
,
0
4
2
27
-
NUMBER OF FEEDING ATTACKS
LF:.
MARKED SNAILS
UNMARKED
FIG. 1. Summary of 632 observed feeding attacks by all Nucella emarginata.
- - - percentage cover estimates from 100 random points/m2.
snails, 104 were observed through two or more feeding
attacks in the field during the 4-mo study. Feeding
sequences for the 51 snails observed through five or
more sequential feeding attacks (Table 3) illustrate two
major points.
1) Within each study site and between individuals
close to the same size, the diets chosen by some individuals differ markedly (Table 3). For example, in
the first two diet sequences presented in Table 3, snail
61 ate only barnacles (3 spp.), and snail 51 ate only
molluscs (3 spp.); in the 3rd and 4th sequences snails
52 and 60 ate both barnacles and molluscs but in different proportions. At site B, individuals predominantly ate barnacles, yet some individuals ate more of
one barnacle species than another. For example, snail
6 ate at least three species of barnacles: Balanus glandula, Chthamalus spp., and Tetraclita rubescens, while
snail 49 ate only the one species, a diet consisting entirely of Balanus glandula.
2) Individual snails showed a high degree of consistency in their diets. Populations of N. emarginata at
sites A and B attacked seven and four prey species,
respectively, but no individual snail observed in the
entire study ate >three prey species (Table 3). Moreover, of the individual predators at site A, 6 snails ate
three prey species, 11 snails ate two prey species, and
3 snails ate only one prey species. At site B, 5 snails
ate three species, 14 snails ate two species, and 12 snails
ate one species. At site A, 2 out of 20 snails (51 and
26) ate only molluscs, 8 fed only on barnacles (61, 11,
72, 53, 20, 66, 49, and 24) and 10 fed on both barnacles
and molluscs (52, 60, 27, 14, 4, 65, 21, 7, 18, and 69).
All of the snails at site B ate only species of barnacles
(though some limpets were eaten by individual N.
emarginata with < 5 observed feeding attacks).
The apparent specialization by individuals on dif-
3112
25
337
densities of prey changed to percentages,
ferent prey could simply be shaped by a patchy distribution of prey and predator. However, this did not
cause the patterns observed in my study. Approximate
routes of each marked snail indicate that a variety of
potential prey was encountered between successive tides
(Fig. 2). Routes of snails 66, 52, 51, and 26 are representative of the maps I have for all individuals. While
the lines do not show the exact routes traveled (snails
may wander in a complex way when submerged), they
summarize a snail's movement over rock surfaces. The
maps show that sequential attacks on the same prey
species are not simply artifacts of feeding through a
prey patch consisting of a single species. Two individuals fed on the same surface area but chose different
prey species (Fig. 2A, B). Other examples of individuals
choosing different prey from the same surface are listed
in Table 4. Snail 51 consistently fed mostly on limpets
even when it moved across different rock surfaces (Fig.
2C). Similarly, snail 26 (Fig. 2D) always fed on mussels,
despite moving over different rock surfaces.
To test more carefully the hypothesis that individual
snails are not choosing prey simply in response to the
numbers of prey each individual contacts, I carried out
the following analysis. In some feeding sequences a
predator attacked the same species of prey several times
in succession, then changed to a different prey species
for another series of attacks (see individuals 61, 27, 65,
21 in Table 3A; individuals 6, 2, 39, 52, 21, 47, 29 in
Table 3B). To test whether changes in individual diets
were correlated with changes in availability of prey, I
examined the sections of each dietary sequence in Table 3 that had no missing observations. From these
sections I examined the cases where diet changed from
one species to another. In such instances, the degree of
change in the availability of the two prey species was
examined preceding each attack. The degrees of change
June 1986
PREY SELECTION BY INDIVIDUAL SNAILS
in the availability of the selected pairs of prey species
are plotted in Figs. 3 and 4. Availability was estimated
from both percentage cover and the 2-cm transect
counts. No consistent changes in patterns of abundance
of prey species accompany changes in diets, using either
measure of relative abundance. If changes in diet correspond to changes in availability of prey, one would
expect to find a large number of points located in the
"decreasing PREY I; increasing PREY II" quadrant of
Figs. 3 and 4. One would also expect the "increasing
PREY I; decreasing PREY II" quadrant to be without
points. In the transect analyses (Fig. 3) points are scattered across the quadrants, suggesting that changes in
relative abundance of prey do not precede changes in
diet. In the percentage cover method of determining
relative abundance (Fig. 4), 10 out of 16 points fell on
the origin at site A and 19 out of 23 points fell on the
origin at site B, indicating that in most cases where
diet changed, percentage cover values of prey did not
change. Changes in abundance of one prey species are
not significantly correlated with changes in the other
species (P > .05, Olmstead and Tukey's corner test
for association, Conover 1971). It appears that changes
in relative abundance of prey do not precede changes
in diet.
How likely is it that the diet observed for each individual is obtained by random foraging through available prey? The probability of getting a diet consisting
of the observed numbers of individuals of each prey
species was calculated incorporating the relative abundance of prey available in the study areas (see Methods). Probabilities presented in Table 3 include not
only the probability of the observed diet, but also the
sum of the probabilities of diets more or equally specialized in comparison to the observed diet. These
probability values are conservative because they account only for the number of prey species in the diet,
not the order in which those prey species occur. All
but one diet (snail 7) at site A and four diets (snails
23, 21, 61, 40) at site B have probabilities of <.05.
Hence it is very unlikely that the observed patterns of
species eaten by individuals are simply an artifact of
sampling from the available prey.
Finally, is it possible that the differences observed
in this study are a consequence of sampling at low tide?
Fairweather and Underwood (1 98 3) point out that when
continuous processes can only be observed intermittently, the investigator's observations are biased towards the activities that are longer in duration. For
feeding studies, when handling times differ between
species of prey, the prey that require long handling
times are more likely to be observed. In my study,
handling times are indeed different for different species
of prey. The length of time Nucella emarginata remains
with its prey is related to the size and species of the
prey animal (Table 2). Chthamalus spp. and Collisella
scabra were eaten most quickly while snails remained
for the longest time periods with mussels, Mytilus californianus. This indicates that I probably missed some
803
small prey consumed completely at high tide. Yet this
problem cannot explain differences between individual
diets, because prey requiring short handling times, such
as barnacles and limpets, do show up frequently in the
diets. The diet sequences of prey requiring longer handling times, such as mussels, could conceivably be
missing barnacles eaten at high tide (snails 51 and 52,
site A), but I still maintain that individuals do not eat
similar diets. It would be very unlikely that within long
sequences of barnacles or limpets the individual would
have eaten mussels at high tide and not remained with
a mussel into the following low tide (snails 61, 11, 7,
53, 18, 20, 66, 49, and 24, site A). Intermittent sampling could bias the diet data toward interindividual
differences if some individuals eat certain prey species
only when they are submerged and eat other species
when exposed. While I recognize this possibility, it
seems clear that individual N. emarginata are not all
foraging in the same manner.
DISCUSSION
Observations of serial feeding episodes made by individual Nucella emarginata indicate that members of
a population may choose different diets from the same
natural array of prey species in their environment.
Feeding observations also show that within many individuals' diets, prey choice is consistent, at least over
time periods <3.5 mo. Relative abundance and accessibility of prey may shape the diets of predators
(Murdoch and Oaten 1975, Hassell and Southwood
1978, Krebs 1978). However, this study demonstrates
that differences between individual snail diets are not
necessarily linked to the relative abundance of prey
that an individual contacts as it moves across rock
surfaces. Hughes and Dunkin (1 984b) also report that
diet preferences of Nucella lapillus in laboratory choice
experiments were not changed by short-term fluctuations in relative abundance of prey species. In Washington State Palmer (1984) found that Nucella emarginata and two other species, N. canaliculata and N.
lamellosa, did not simply eat whatever potential prey
they happened across, nor did snails choose prey in
proportion to the relative abundance found in their
surroundings.
Sequential feeding attacks on one prey species when
other prey are available have been reported for a wide
range of animals (Werner et al. 1981, Bayliss 1982,
Hall et al. 1982, and references therein). Several interrelated factors may contribute to sequential feeding:
experience in handling prey, ingestive conditioning,
and physiological factors.
Experience may help predators find and handle prey
more efficiently as they eat more and more of the same
prey (Heinrich 1976, 1979, Laverty 1980, Werner et
al. 1981, and references therein). Feeding experience
increases both feeding rate and prey preference in carnivorous snails, Polinices duplicates (Edwards and
Huebner 1977) and Nucella lapillus (Dunkin and
TABLE
Ecology, Vol. 67, No. 3
LANI WEST
804
3.
Sequential feeding attacks made by individual snails at sites A and B.
Nucella
Code Size
no.t (mm)0
Elapsed days following first observation of feeding
40
20
Sequence of prey eaten, site A*
- - - - - - - - - P - - I - - PP
61 23.5 B '
B - - - - - - - S - - - - - I- - - - - - - 51 29.0 S - - - - - - ' ' '
- - - - - - - Pp - - - - - 52 24.5 P - - - - - - - - - - - - - - - - - - 60 27.0 P-'''''''
- - - - B
- C - - - - - '' -B
11 24.0 B - - - - - - - - ' M- - - M - - ' P- - - - Pp - P- 27 24.0Mmm-M' ''''''''-M
-M26 24.5 Mmmmm - - 'M - - - - - -'
- - - - - - - - - - - - - - - - - ' 14 26.0 Mm m - - - - - - - - - - - I I I
4 26.0 Mm- - - - - - - - - - - - - ' '-' ' ' - - - - - - - - - I I
- - - Mmmm ' . . M - - - ' - - - - P .'
65 25.5 M- - -'''''''
- - - ' '-P
-B B'
72 26.0 T ' ' ' - - - - - - - - - - MM - -B -B21 27.5 P - P - - '
B --C
-B - -B - - - - 7 25.5 C'
' -'' - ' S
(3) [6]
- - - - - - - - - - - - - - - - '''''
53 24.5 B'
- -- - S P - 18 26.0 S P p pp
' ' ' '
' '-'- - - - - Mmmmm
69 27.5 P -- '''B
(2)[5]
- - - - ' - - C
20 23.0 B - -- - B b - - -B- - 'B- - - - - - -''''''''''''''''66 25.0 B
49 25.5 B B - - - - - - - - - - B ' ' - - - - -- T - - - - - - - ' B
(2)[5]
24 23.5 B '' '' ' --BC - ' - ' B - - - - - - - - - - - - - - - - - B - Total = 20 individuals with ?5 feeding occurrences
A.
- P l
- - -
B
- B - S - - L - - - - - - - -'
' ' --Pp
-Mm- Pppp
- - BBB
- - - - - - - - - - - - - - - I - - ' .-' . - . .
' ' ' ' -. - . .
B
- S
- - - T
- -M- P- P' ' ' ' ' '
. .
-- - -- B.
(3)[6]
. .
.
-
B - B - - - Bb -Bb
(2) [5]
' ' Mm - P
- B
B - - B
- - ' -
(1)[5]
(2) [5]
B. Sequence of prey eaten, site Bt
- - -''
' ' ' - - - -B
-B6 26.5 C - - - - - - ' - T t T B - B - - - -B
T - - -BbBB'
- B
- - - - B - - B - - - - - - - - - - B - - - - - - - B''
- 49 25.5 B - - Bb 'B
- - - -- -T '
Bb-B ----B
18 29.0 T t t - - B - - - B- - - T t t - - ----C- - Bb- B - - - - - - - - 70 27.5 B - - - - - - B-B- B -' - - - - - - Bb - - T - - -- -'B --- - -Bb'
''''''- - C - - B
26 24.5 T - - B '-' - - - - B - Bb b b ' B - - - -B'''
-- - - - - - - - T t t - - - - - ' ' - - - - - - 2 25.0 T t t t - - T ' --T'
- - - - - - - - - - B '
- - - - - - - - - 43 27.0 T - - T - - - - B b T - - - B ' - - - - - - - - BT - - - - - - - - - - - - - - - - - B - B B - - - ' ' ' ' ' ' ' ' '
5 24.0 T- - - - - - - - - - - B ' B - - - - B - - - - ' - - B- - - - - B
- - - - - - - - - - Bb - - - -B - - - - - - B
B
54 27.0 B '' '''
' ' - - - - B - - - B
67 26.0 B--B - - 'B B BBB'
(1)[9]
12 26.5 B B B - - - - B- B B ' B b b - - - - - - - - B - B
(1)[9]
39 28.0 T - - - - - - - ' - - B b - - - ' BT - - T - - - - T - - ' - B - - - - - - ' - - - - - - - - - - - B
4 30.0 B - - - B - - ' - - - B - - Bb - - B - - - - - - - - - - - - - - - - B - - - - - - - - B - - - - 'B - B
60 24.0 Bb b - - - - - - - - ' - - - - - - - - - - - - - - - B- B b - '- - - - -Bb-B55 28.0 B - - - - - - B- B- - - - - B - - B ' ' B - ' ' ' B
(1)[7]
- - - B
62 25.0 BB - B B B - - T - - ' ' ' ' - - - - - - - - - - - - - (2) [7]
- -B(3) [7]
23 26.0 B - - - C -' - -B- - B - - - - B - - T
14 26.0 TB - - - - - - - B- - B - Bb - B - - - - ' - - - - B- - - - - (2) [7]
63 28.5 B B B B B - - - - - B
(1) [6]
.
(1) [6]
34 24.5 B ' '.' . .
- B -Bb - B - - - - - - - - - - BB
59 26.0 B - Bb - - - B- -B ' B - - B
(1)[6]
- - - - - - - - - B
7 25.5 B - - - - - B -B -B - - - - - - - - - B '
- - - - - - - - - - (1)[6]
I' - - - - - - - - - - - - - - - - - - - - - BT - - - - - - - - BB
51 27.0 B - - - - - - - - B'
B
(2) [6]
52 24.0 B - - - - - - - - T 'T t t - - - - - - B b - - - - - - - - - B - - - - - B
- - - - - - - 21 25.0 T t - - - - - - - - - - - - - - - - - - - - BBC ' C - - - - - - - - - - - - ' - ' - 'B' BB -Bb- ' ' B
13 26.5 B '''
(1)[6]
61 28.0 B - - - - - - - - B B C ' - - - - - - - - -- B - - (2) [5]
40 27.0 B 'C - - - - - B - - - B - - B
(2) [5]
' ' ' - - - - - - - - - - - - - - - - B - - - - - - B '- - - - - - - - - - - - - - - - - - 56 24.5 T -B'
47 24.0 T - - - - - - T - B- - - - - B - B - (2) [5]
-- - - - - - - - B
29 25.0 T - - - - - - - - - - - - TB'''
(2) [5]
Total = 31 individuals with - 5 feeding occurrences
* Symbols indicate the following: B = Balanus glandula, C = Chthamalus spp., L = Collisella limatula, S = Collisella scabra,
M Mytilus californianus, P = Pollicipes polymerus, T = Tetraclita rubescens. Small letters in some of the sequences indicate
continued feeding by a snail on the same prey individual through more than one observation period. - = snail observed but
not feeding, ' = snail not observed, ( ) = number of prey species per individual, [ ] = total number of prey per individual.
t Duplicate Nucella code numbers at the two different sites refer to two different individuals.
t Probability values are the likelihood that the particular diet sequence occurred by random foraging through the estimated
relative abundances of prey species on the natural rock surfaces.
PREY SELECTION BY INDIVIDUAL SNAILS
June 1986
805
Elapsed days following first observation of feeding
80
60
94
- B - B -''
- - ' - - B - CB' - -B
(3)[14]
-M-L - - - - - S - - S - - -Mmmm- - ' ' ' ' '- ------' - - - S
(3)[11]
t-----M---P-Pp---P--P'P--P
--P- ' ' ''' M
-- - t-'
- - -M- -Pp'
Pppp
-(2) [9]
(2) [8]
pp
(2) [8]
--M
(1)[6]
(2)[6]
--------Mmmm-''''---M-M-PM
- -Mm--------------------Pp
- ' - - ---MMm--Mmp
'-------M
(2) [6]
(3)[6]
b
-
(1)[5]
- -
(2) [5]
-Mm-Mm
- - - - - - - - - - -B
B - - - B
B- - B - - ' ' ' ' - - - BB ' '
(3)[10]
- - ' - - - - BBBB (2) [9]
- - - - - - - B - B
b -B b - - - (1)[9]
- - - - - - - C
- - - (1)[12]
- -- - -
T
- -
- - T
(3)[12]
- -
(2) [10]
(2) [9]
-
- - - - - - -
- - - - - - B
B
---
(3) [13]
- -
(2) [9]
(1) [71
(1) [7]
(2)[9]
(3)[12]
Probability
of diet
1.21 x 10-8
4.16 x 10-9
6.38 x 10-"
5.35 x109
2.69 x 105
7.27 x 10-8
1.00 x 10'12
(2)[6]
1.63
1.63
2.04
8.65
6.95
x
x
x
x
x
10-8
10-8
10-7
105
10-2
6.54 x
1W-2
1.00 x
10--4
1.16
6.84
7.00
1.20
8.44
6.57
x
x
x
x
x
x
1.24
7.68
1.98
1.15
1.46
1.47
6.54
2.41
1.31
1.31
1.31
6.54
6.00
6.23
x 102
x 10-5
x 10-3
x 1O-3
x 10-2
x 10-4
x 10-4
x 10--3
x 10-3
x 10--3
x 10-3
x 10-4
x 10-3
x 10-3
103
10-7
10-3
10--4
105
10-3
6.23 x
10-3
1.15 x
10-2
8.78 x 10-2
1.15 x
(2)[6]
--
- - - - B - - -
- - - B
(3)[6]
(2)[5]
Hughes 1984, Hughes and Dunkin 1984a, b). Studies
of bluegill sunfish (Werner et al. 1981) and bumble
bees (Heinrich 1976, 1979) report both sequential feeding attacks on one prey species, and also describe differences between individuals in the same environment.
Heinrich (1976, 1979) showed dramatic interindividual differences, with bumble bees foraging more efficiently on a certain type of flower once they became
10-2
x
x
x
x
x
10-2
1.21 x
10-2
1.32
1.32
1.32
1.32
1.73
3.37
1.32
2.15
2.15
4.28
1.57
1.57
x
x
x
x
x
x
x
10-2
10-2
10-2
10-2
10'
10-2
10-'
10-'
10 2
10-2
10-2
experienced with the flower structure. Specialization
on different prey types within a foraging population
might occur in species of predators whose prey require
contrasting handling techniques but still contain roughly similar rewards.
Nucella emarginata use different attack techniques
to penetrate different species of their invertebrate prey.
They usually drill through the shell at specific locations
LANI WEST
806
Ecology, Vol. 67, No. 3
AA
'
START,
~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~
5~~~~~~~~~~~~~~~~~~~~~~~~4
4
DISPLACEMENT RECORD
\
DISPLACEMENT RECORD
POTENTIAL
PREY
EPRE
POTENTIAL
(G
X
\/
SPECIES
PREY
EATEN
.
SPECIES
BALANUS GLANDALA
A
COLLISELLA SCABRA
POLLICIPES
SCABRA\
.COLLISELLA
.
"
;
MYTALUS
COLLISELLA LIMATULA
t
Lo
CALIFORNIANUS
o
SPP, r.
;xCHTHAMALUS
/
COLLISELLA LIMATULA
\
POLYMERUS
D
\e
TETRACLITA RUBESCENS
'
BALANUS GLANDULA
)rx
SPP,
:--CHTHAMALUS
\
0.5 mEESCENS.
SCA TETEACLETA
LSCALE m
@
'7
MYTILUIS CALIFOENIANUS
POLLICIPES POLYMERUS
\-
TETRACLITA RUBESCEN5
0.
AD~~~~~~~~~~~
4
b
5A
NI
sA1tX D
E-\R
I
A6t',\<
DISPLACEMENT RECARD
PATENTIAL
PREY
PREY
EATER
XC
DISPLACEMENT REGARD
BALANAS ALANDALA
?
A
IG
COLLISELLA LIMATALA
TETEACLITA RUBESCENS
0.5 m
CHTHAMALAS SPP.
\CALLISELLA
D
2*- A
a5
\ '
9
_
\
)
MYTILAS CALIFARNIANAS
PALLICIPES PALYMERAS
TETRACLITA RABESCENS
D20114
tSCALE
0.5
m
x
\
g5
t
v
*-
.C.
\'
@
\o
t~~~
Ds
y
LINATALA
COLLISELLA SCABRER.
A
.\M.MRL
\
\-
SPECIES
ALANAS GLANDALA
J
{<
\
TAT
PREY
EATEN<
B
.
t-
CALLISELLA SCABRA
PALLMYICIPS
PELYMERNANS
POLYMERUS
POLLICIPES
PATENTIAL
PREY
XE
SPP.
0/t
SCALE
A
A
SPECIES
'.'CHTHAMALAS
~~~~~~~~~~~~~~~~~~~~~~
\
2
,
\<
\
\,
<
:
FIG. 2. Net displacement record and sequential feeding attacks made at site A by (A) snail 66, (B) snail 52, (C) snail 51,
and (D) snail 26. Numbers along the snail path indicate the number of observations the snail remained at the specific location
indicated. Estimates of relative abundance of prey from each rock surface are represented in the figure to give an approximate
indication of prey availability.
June 1986
PREY SELECTION BY INDIVIDUAL SNAILS
4. Portionsof the diet sequencesof individualsthat
moved acrossand chose prey on the same 2 x 0.5 m rock
surface.
807
TABLE
Study
site A
SurfaceI
SurfaceII
Snail
number
61
4
52
60
II
Section of
prey sequence
BBBBBCBB
MMPMM
PPPTMPPPP
MPMPMP
BBBBB
Dates
(all 1978)
16 Apr-i 1 May
14 Apr-18 May
18 Mar-18 Apr
17 Mar-20 Apr
29 Mar-14 Apr
W
PREY 11
|
W~~~~
30
Wa
z
o)
-3
cu
n=I9ot(0,0)
D
z
- ~30
Z
PREYI 4
So
a.
0
z
0
PREYI4
PREYIt4
PREY I
30 PREY 114
-
PREYI Is
PREY II 4t
CHANGE IN PERCENT
ABUNDANCE OF PRE Y I
FIG.4. Changesin the availabilityofpreyprecedingchanges
in the diet sequenceof individualNuce/la snails. Abundance
of a prey species was used as a measureof availability,as in
Fig. 3, except that abundancewas based on percentagecover
by a speciesin 10 -cm2quadrats.Casesof changein diet from
PREY I to PREY II are plotted to show the changein abundances of those species in the rock surface quadrats where
PREY I and II were eaten. Labelingof figurequadrantsas in
Fig. 3.
Z
30.
30
*
L0
PREY I 4'
PREY 1It
'
PREY
I 4
Pk
0 PREYII +i
PREYI
PREYII '
PREY 11 4,
4
. * n lOoa t (0,O)
-
0
o
PREY I+
PREY1EI.
PREY I4'
- PREYIII
-30
L.
m
on the morphologically diverse prey species. These specific handling techniques, along with individual consistency in prey choice, may be analogous to the bumble bee foraging patterns described by Heinrich (1976,
1979) and Laverty (1980). Since carnivorous snails improve their attack techniques with increased experience
(Edwards and Huebner 1977, Dunkin and Hughes 1984,
Hughes and Dunkin 1984 a, b) this is a possible mech-
0
PREYI jJ
H
W
z
3
PREYI
*
PREYII4'
PREY I 4
PREY It
anism that could encourage interindividual differences
in diet.
w *N
Feeding experience may also influence foraging behavior by chemical means. Wood (1968) describes the
.
:
_30
*
30
phenomenon of "ingestive conditioning" in a carniv-30
Z
W
orous snail. Urosalpinx cinerea collected from areas
CD
where they fed predominantly on one species of prey
Z
chose to follow the effluent of that prey when offered
I
PREYI
water streams containing different species of prey. A
-30 PREYI 4'
PREYI
PREYII4
f
snail's preference for the effluent of a species of prey
could be changed by feeding it a restricted diet of another
CHANGE IN PERCENT
species. Ingestive conditioning was also demonstrated
ABUNDANCE OF PREY I
in laboratory work with Nucella lapil/us (Dunkin and
FIG.3. Changesin the availabilityof preyprecedingchanges Hughes 1984, Hughes and Dunkin 1984a). In these
in the diet sequenceof individualNucella snails. Abundance studies and those done by Wood (1968), interindividof a prey species, stated as a percentageof all potential prey
speciespresent,was used as a measureof availability.Where ual differences in food choice were not investigated.
Physiological phenomena, such as a predator prodiet changed,the abundanceof each prey species was measured in a 2 cm wide transect immediately before PREY I ducing a digestive or detoxifying enzyme for a specific
was eaten,and measuredagainjust beforePREYII was eaten. type of food (Kitting 1980), could act in addition to
The differencebetweenthe two measuresof PREY I (x axis) both ingestive conditioning and learning. Genetic variand the differencebetween the two measuresof PREYII (y
axis)areplottedabove as points(x, y). Labelsin eachquadrant ability may also affect the ability of individual predcharacterizethe changein abundanceof PREY I and PREY ators to locate prey (Arnold 1981). Whatever the mechII in that quadrant;Tincreased,I decreased.
anisms are, fixed specialization is probably not an
Z..
808
LANI WEST
advantage in most environments, because the animal
is not able to cope with change in its surroundings.
Heinrich (1976, 1979), Laverty (1980), and Werner et
al. (1981) all describe circumstances where their respective study animals maintain short-term specialization for feeding efficiency, yet still retain the flexibility to change to another food type when necessary.
It is difficult to predict whether exceptionally long-term
feeding studies of these organisms would show an increase or a decline in the degree of interindividual differences. If comparison of snail diets over the long term
showed less variation between individuals, the shortterm individual consistency reported here could still
be important to the efficiency of feeding individuals.
The present study was not designed to test optimal
foraging theory, but it is relevant. Where optimal foraging studies usually predict the behavior of the average individual in a population, my study was designed to examine differences between individuals in
foraging behavior. Because diets of individuals within
the same location were found to differ, the implicit
assumption of simple optimal foraging models, that all
individuals in a population evaluate prey according to
the same hierarchy, should be questioned. Some researchers in optimal foraging theory are now taking
this idea into account by considering the effects of experience and learning on the behavior of a forager
(Hughes 1980, McNair 1981).
We do not yet have a broad enough sample of investigations exploring interindividual variability to
make generalizations about the degree and extent of
its occurrence. Most studies where foraging individuals
have been compared within a population report that
there is a high degree of interindividual variability (see
references in Hassell and Southwood 1978, Arnold
1981, Werner et al. 1981). However, Kitting (1980)
reports that individual limpets maintained similar
mixed diets of algae on different rock surfaces.
This study documents another organism that shows
variability between individuals in foraging behavior,
and demonstrates that this variation is unlikely to be
caused by a simple relationship between predator distribution and relative abundance of prey, or sizes of
prey and predator. Future studies exploring the establishment of individual differences subjected to changing environmental conditions, or the heritability of
preferences when individuals within a population show
variability, will be important in distinguishing the roles
of the many influences acting on foraging behavior.
Other experiments could be designed to explore growth
rates and reproductive success of individuals that specialize in diet compared to those that generalize within
a local population. Although the major questions of
many ecological studies are not directed toward variation between individuals, a focus on this variability
may suggest new hypotheses and may help to integrate
studies of evolutionary processes, physiology, and ecology.
Ecology, Vol. 67, No. 3
ACKNOWLEDGMENTS
I thank Donald P. Abbott for inspiration, the suggestion of
following individuals, and assistance in all phases of this research. Thanks also go to James Watanabe, Charles Baxter,
Christopher Kitting, Anson Hines, Robin Burnett, Bruce
Menge, Jane Lubchenco, Teresa Turner, Christopher Marsh,
Steven Gaines, Carla D'Antonio, Monica Geber, Edwin Bourget, Harilaos Lessios, John Christy, and Terence Farrell for
useful discussion and comments on early drafts of this work.
I thank James Watanabe, Steven Gaines, and Terence Farrell
for statistical advice. I thank John Lucas for computer assistance. Comments from anonymous reviewers and R. T. Paine
helped to improve the manuscript. I thank the faculty and
staff of Hopkins Marine Station for use of facilities. Colin
Pittendrigh, Judy Thompson, Alan Baldridge, Susan Harris,
Sharon Nugent, Chris Patton, and John Kono provided special assistance.
LITERATURE CITED
Abbott, D. P., and E. C. Haderlie. 1980. Prosobranchia:
marine snails. Pages 230-307 in R. H. Morris, D. P. Abbott,
and E. C. Haderlie, editors. Intertidal invertebrates of California. Stanford University Press, Stanford, California,
USA.
Arnold, S. J. 1981. Behavioral variation in natural populations. II. The inheritance of a feeding response in crosses
between geographic races of the garter snake, Thamnophis
elegans. Evolution 35:510-515.
Bayliss, D. E. 1982. Switching by Lepsiella vinosa (Gastropoda) in south Australian mangroves. Oecologia (Berlin) 54:
212-226.
Connell, J. H. 1961. Effects of competition, predation by
Thais lapillus and other factors on natural populations of
the barnacle Balanus balanoides. Ecological Monographs
31:61-104.
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