ABSTRACT
Foraging behavior of Ocenebra circumterta, an abundant predatory gastropod in
the intertidal zone at Hopkins Marine Station, was studied. Ocenebra in the field were
observed consuming barnacles, small limpets, tube worms, and mussels, with two
barnacles, Tetraclita squamosa and Chthamalus spp. composing 85% of their diet. As a
population, Ocenebra appear to consume prey proportional to its abundance in the field
This is consistent with random prey selection. However, snails marked and monitored
over à five week period through 2 to 4 feeding cycles showed consistency in prey choice
that differed from the population average. Prey items chosen by each individual were
also consistent with a particular vertical zone in the intertidal.
Ocenebra occur vertically from the subtidal to approximately 45 feet above Mean
Lower Low Water (MLLW). This range encompasses 3 major zones, divided according
to domination by algae, Tetraclita, or Chthamalus. Marked snails remained within the
vertical zone corresponding to their choice of prey at a much higher rate than would be
expected if the individuals moved about randomly. Two possible conclusions are that
Ocenebra stratify according to prey type in a given vertical zone, or that Ocenebra
stratify for non-foraging reasons. Evidence for the former is that in laboratory tanks with
4 types of prey items, all 8 individuals monitored throughout 3 to 5 feeding cycles chose
prey consistent with a specific zone in the intertidal. This could imply that learning.
conditioning, or genetic variation in present in Ocenebra circumtexta, and could lead to a
competitive advantage over other predatory snails in the intertidal.
INTRODUCTION:
The intertidal zone is stratified into many different microhabitats. Lower regions
on the shore are submerged a high proportion of the time, providing a habitat for species
susceptible to desiccation such as tube worms and various algae. High intertidal zones
may be exposed to air for a longer time than they spend submerged. This harsher habitat
selects for species with a variety of traits, including the ability to resist desiccation
(Ricketts et al. 1985).
Some species have a range encompassing more than one intertidal zone beçause
they are able to withstand the various stresses accompanying different zones. As a
species, these habitat generalists often consume more than one type of prey. Two
extreme possibilities exist with regard to prey choice among species found in more than
one zone. Individuals may truly be habitat generalists, travelling across all zones in the
species range and consuming many different types of prey. Alternatively, it is possible
that individuals specialize on a subset of the species diet, leading to interindividual
differences in prey selection and stratification corresponding to prey abundance. Grant
(19/1) explored this concept as it relates to birds, pointing out that populations can be
composed of members that" differ in their modes of exploitation, being either specialists
or generalists" or "individuals that are similar... and are all generalists." The only way
to distinguish between these two possibilities is to observe individuals.
West (1986) found that interindividual variation exists within a population of the
predatory gastropod, Nucella emarginata. Individuals in her study consistently chose the
same type of prey, bypassing some prey species and actively selecting others. She
suggests that learning or genetic conditioning may occur in N. emarginata. Hughes and
Dunkin (1984) showed learning to be the basis of these interindividual differences. In
their study, Nucella lapillus, another predatory snail species, was maintainted on one type
of prey for 60 days and subsequently showed a preference for that prey. This type of
learning may occur in the field, as well.
Ocenebra circumtexta, a predatory gastropod, has recently increased in
abundance at Hopkins Marine Station in Pacific Grove, California. Ocenebra are
commonly found in several zones of the intertidal, ranging from Mean Lower Low Water
(M.I.W) to 16 above MLLW. This range encompasses several distinct microhabitats
with different prey assemblages in each zone
Ocenebra circumterta is not a widely studied organism. Another gastropod of the
same genus, Ocenebra lurida, consumes mainly limpets and barnacles, and occasionally
mussels (Palmer, 1988
This study examines population as well as individual prey selection in Ocenebra.
and differences between the two. I also explore movement patterns of individuals
between zones in the intertidal, and the correlation between movement and prey choice.
The results indicate that there is indeed a correlation between prey choice and zone
localization by individual snails, and that variation in individual prey selection may exist
MATERIALS & METHODS.
Intertidal Habitat
I divided the Ocenebra intertidal habitat into three zones according to species
characteristic of each zone. The lowest zone, the algae zone, ranges from t2 fet above
Mean Lower Low Water (MLLW) to the subtidal. This region is mostly covered by
fleshy algae, with scattered volcano barnacles of the species Tetraclita squamosa and
clumps of the tube worm Phragmatopoma caljfornica. Above the algae zone is the
Tetraclita zone, extending from 1.5 to 4 feet above MLLW, in which the barnacle
Tefraclita is the dominant species. Mussels (Mhtilus caljfornianus), and limpets (Lotia
paradigitalis), occur in the upper parts of this zone, and Phragmnatopoma and other tube
worms are found in the lower parts. The highest zone occupied by Ocenebra, the
Chihamalus zone, extends from 3 5 to 6 feet above MLLW and is composed mosty of
the acorn barnacles Chthamalus sp. and Balanus glandula, as well as several species of
limpets (Macclintockia scabra, and Lottia paradigitalis)
Ocenebra Feeding Habits
Criteria for feeding in this study was evidence of drilling into the prey item, or
seeing the snail's proboscis extended to consume the prey item. Because L was not
always able to see a hole or the proboscis, a secondary set of criteria to determine feeding
was developed. One secondary and not always conclusive indicator of feeding in
Ocenebra was strong adhesion to the prey item, which usually accompanied drilling or
feeding. However, this behavior was also exhibited by non-feeding snails during dry
afternoon low tides, which may indicate that it is not solely a predatory behavior.
Remaining with a prey item for 2 or more consecutive days was also interpreted as
feeding.
Population Average
Information on the average diet of the Ocenebra population was gathered by
placing sixteen O.25m' quadrats in areas with three or more Ocenebra. Feeding status
and prey choice of Ocenebra were recorded, and estimations of prey species abundance
by percent cover for species in high concentrations, or by number of individuals for less
abundantspecies were made. The numbers of indvidual prey items per quadrat uere
translated into percent coverage of the quadrat surface area. Iasumed a circular shane
for the base of barnacles and limpets, and used a mean base diameter gathered from
sampling 20-30 organisms to calculate basal surface area for an individual. This
information was then translated into total surface area coverage and percent coverage by
each prey species. Data for individual quadrats was averaged to characterize the
intertidal habitat where Ocenebra are found. The average percent cover for each species
was divided by the sum of all available prey by percent cover to yield relative prey
abundance for each species.
Study Site
Studying individual snails was necessary to discover whether interindividual
differences exist in prey choice, or whether individual snails conform to the population
average. Ioriginally selected two field sites in the rocky intertidal of Hopkins Marine
Station for their high abundance of Ocenebra, as well as their accessibility during loy
tide. One of these study sites was later dropped, as it lacked the vertical range of the
other sfudy sife and snails dispersed too far from the original study area to relocate
reliably.
The remaining study site was divided according to species composition into the
three zones mentioned previously (algae, Tetraclita, and Chthamalus zones), and percent
cover of each zone estimated. I found that the algae zone and the Tetraclita zone each
spatially cover 40% of the Ocenebra habitat in the study site. The Chthamalus zone
composes the remaining 20% of the Ocenebra habitat in the study site
Marked Individuals
1 marked 26 snails in the vertically stratified study site, mostly in the Tetraclig
zone. Aseries of thre colored nail polish stripes allowed identification of individual
snals throughout the study period. Nail polish occasionally had to be reaplied but was
relatively hardy in the field Marked snails were observed almost daily at low tide fora
makimum of 28 observations over a S-wek period. Feeding behavior at the time of
observation as well as snail location on a map of the study site was recorded
Nine additional Ocenebra initially observed in the Chthamalus zone of the study
site were also marked and observed to assess whether snails move randomly throuch their
habitat, or whether individuals localize to a particular zone. Snail positions were
recorded during 10 observations at low tide over a course of 2 weeks
Laboratory Study
Laboratory tanks were set up to examine individual prey choices in a controlled
environment where snails had a known composition and density of prey. Four replicate
tanks were establis hed containing 8 randomly selected Ocenebra in each tank, and knoun
relative abundance of 5 prey species. The number of these individuals was converted
into percent cover of each prey species as described previously, and calculated relative to
total prey cover in each tank. Prey species included (with relative abundance by area
cover in parenthesis) Tetraclita (64%), Chthamalus (8%), Lottia paradigitalis (690).
Macclintockia scabra (7%), and Mytilus californianus (19%). Laboratory tanks were
monitored daily to record behavior of each Ocenebra. Individuals were handled as little
as possible, to minimize disturbance. Therefore, feeding was usually determined by an
individual's presence on a prey item for more than a day, and was confirmed by evidence
of drilling into the shell or of loose opercular plates in barnacles,
RESULTS:
Ocenebra were observed in the field handling and consuming prey, inchuding
lefracita quamosa, Chuihamalus spp, Balanus glandula, Lotia paradigialis, Abtilus
caijornianus, Phragmatopoma caljfornica, as wellas several other unidentified ube
worms. This information is based on 156 snails observed, 44%6 of which were feding.
Ocenebra atack prey both by drilling with the radula through the prey's shell as wellas
by reaching through the opercular plates of barnacle species. The proboscis is then
everted into the hole and the flesh of the prey is rasped out. A behavior characteristic of
feeding is wrapping the foot around part of the prey item, allowing the radula to serape
between the edges of the foot.
Data collected from quadrat studies of Ocenebra shows a correlation betwueen
Ocenebra prey choice and abundance of the prey item in the field (Table 1). Tetraclig
and Chihamalus, which combine to make up 85%6 of Ocenebra's diet, are consumed at a
frequency nearly equivalent to their relative abundance. This may indicate that Ocenebra
are feeding at random, consuming prey in the abundance at which it occurs. Some of the
less common prey species are not consumed at their abundance in the field. Despite its
relatively high concentration in the Chthamalus zone, the limpet Macclintockia scabra
was not observed as a prey item of Ocenebra in the field (Table 1), yet laboratory
experiments show that M. scabra is indeed consumed by Ocenebra (see below)
Ocenebra observed in the study site seemed to show consistency in prey choice.
Of 26 marked snails, 9 were observed through 2 to 4 feeding cycles (Table 24). Each of
these appeared to choose prey consistent with one of the three habitat zones. Snails l.2.
3, 4, 5, 6, 8, and 9 ate Tetraclia and Phragmatopoma, which are both found in the
Tefraclia and algae zones. Snail ? consumed both Tetraclita and Chuhamalus, found on
he border betwen the Chhamalas and Tetraclia zones. Italso appears that indviduals
are not choosing prey consistent with the average population of Ocenebra (Table 28)
A map of snail movements through the study site shows the localization of
particular individuals to certain zones (Fig. 1). The zone individuals stratifuy to also
corresponds with their prey choice (Table 34). If snails moved randomly throuch the
study site,20%0 of the time they should be observed in the Chhamalus zone, 40%6 of the
tume in the Tetraclita zone, and another 40% of the time in the algae zone. Based on
snail locations during low tide, this is not the case (Table 3). The map of snail
movements (rig. 1)also shows the vertical and horizontal distance that several Ocenebra
traversed Snail 8 has a wide vertical range, extending from the lower boundary of the
Tefraclita zone, to the upper boundary, a distance of about 3 feet. Snail 9 shous a pattem
of horizontal movement, ranging over 6 feet yet remaining within the Tetraclita zone.
These data show that Ocenebra are not limited to a given habitat zone simply by their
mability to traverse the distance into another zone. Individuals who ranged far across one
zone and didn't venture into another zone show evidence that some individuals may
localize to a particular zone. Ocenebra marked in the Chthamalus zone also exhibit this
strong tendency to remain within one zone (Table 3B)
In the laboratory tanks, individuals tended to choose prey consistent with a zone
in the intertidal (Table 4). Prey items are not chosen by individuals acording to relative
abundance in the tanks (Table 4B). Snail l ate only Chthamalus and M scabra, both
found almost solely in the Chthamalus zone. Snails 2, 3. S, and 6 consumed only
Teraclia, consistent vith the Teraclia or algae zone. Smais 4 and 7 chose prey found
in the intersection between the feraclita zone and the Chhamalus zone. Althouch these
data are not conclusive because the original location in the interidal of the Ocenebra
prior to placement in tanks is unknoun, it does appear that the individuals are choosing
prey consistent with a particular zone in the intertidal.
Cumulatively, these data seem to indicate that individual Ocenebra localige to
parnicular zones in fhe intertidal, and that they consume prey consistent with a particular
zone in the intertidal. This corelation is further examined in the discussion
DISCUSSION:
Observations of Ocenebra circumteria indicate that individuals tend to consume
prey consistent with a specific intertidal zone, and that Oeenebra localize to a particular
zone in the intertidal at a much higher frequency than expected if individuals moved
fandomly. This is true for individuals marked in both the Tetraclita zone as wellas the
Chthamalus zone.
There are several explanations why individual snails localize to particular zones
The first possibiliy is that Ocenebra stratifj acording to prey assemblages in different
zones. Burrows and Hughes (1991) found that doguhelks (Nucella lapilie) transplanted
between sites with different prey availability retained a slight preference for their original
prey type. The preference, he suggested, is largely a reflection of prey availability at a
snail's original site. Similarly, Ocenebra may remain in certain localities based on prey
assemblages. This may imply that Ocenebra learn to prefer one prey over another, then
localize according to this preference.
Another explanation for differential localization by individuals is based around
genetie diffrences between Ocenebra in different zones, It is posible that individuals in
ine Chuihamalus zone have genetically increased tolerance for desiccation or temperature
stres, and thus localiae to the Chuthamalus zone to avoid competition for resourees or
exposure to predators. If this is the case, individuals simply consume prey acording toits
avallability within their zone. Hughes and Taylor(1997) found that doguhelks Oucela
lapilus) from different populations have slightly different shell morphologies. This
genetically transmitted trait corresponds with the amount of wave exposure the
population experiences. Whether Ocenebra at Hopkins Marine Station is composed of
two or more genetically variable sub populations with one population localizing to the
Tefraclita zone, and one to the Chthamalus zone remains to be examined
Variation in Ocenebra feeding behavior also occurs. Ocenebra were observed
attacking Teiraclita in two ways: by drilig into the side of the bamnacle, and by priging
open the opercular plates. These two methods of handing prey were observed at
approximately equal frequencies both in the laboratory and in the field. In the laborator¬
tanks, however, individuals never drilled all the way through the barmacle shell wall.
Several individuals had an established patter of drilling first, and then consuming the
Tefraclita by prizing open the opercular plates. This pattern remained relatively
consistent over several feeding cycles. In the field, the frequency of success after drilling
through the side of the Tetraclita shell is unknown. Two barnacle shells were found with
holes drilled completely through by Ocenebra, evidence that it is possible to drill hrouch
the side ofthe shell. Ocenebra may be learning how to feed more efficienty by handling
prey in different ways. Further observations of Ocenebra may show an increased
tendency to attack through the aperture of subsequent Tetraclita meals after
unsuccessfully drillig and then succesfiuly prizing open the opercular plates. Dunkin
and Hughes (1984) studied dogwhells experienced with barnacles, and doguhelks
inenpersenced vith barnacles, finding that more experienced indviduals priged open the
opercular plates, whereas inex perienced snails tended to drillthrough the sides of the
barnacles, until they learmed that prizing open the opercular plates is more eficient
Increased observations could lead to conclusions about this aspect of feding in
Ocenebra,
This study provided preliminary data on habitat preference and prey selection in
Ocenebra. More data will allouy better conclusions about Ocenebra behavior and the
correlation between zone preference and prey choice.
ACKNOWLEDGEMENT
T thank Jim Watanabe for his patience and support, and for the suggestion of following
individual snails. I also thank Jessica Davy, for her assistance in lab work.
LITERATURE CITED
Burows, M. T. and R N. Hughes. 1991. Variation in foraging behavior amond
individuals and populations of dog whelks Nacela lapils natural constraints on enero
intake. Journal of Animal Ecology 60(2): 497-514
Dunkin, S DB. and R. N.Hughes. 1984. Behavioral components of prey selection by
dog whelks Nucella lapillus feeding on barnac les Semibalanus balanoides in the
laboratory. Journal of Experimental Biology & Ecology 79(1). 91-103
Grant, P. R 1971. Variation in the tarsus length of birds in island and mainland regions
Evolution 25: 599-614
Hughes, R. N. and S D BDunkin. 1984. Effect of detary history on selection of prey
and foraging behavior among patches of prey by the dog whelk Nucella lapilus. Joumal
of Experimental Marine Biology & Ecology 79(2): 159-172.
Hughes, K N, andM. J. Taylor. 197. Genotype environment interaction expressed in
mhe foraging behavior of doguhelks, Nucella lapillus L), under simulated environmental
hazard. Procedings of the Royal Society of London-Serial B. Biological Sciences,
264(1380): 417-422
Falmer, A. R 1988. Feeding biology of Ocenebra lurida prosobranchia muricacea diet
predator prey size relations and attack behavior. Veliger 31(3-4). 192-203
Kicketts E. F, J. Calvin, and J. W. Hedgpeth. 1985. Between Pacifie Tides. Ed S.
Stanford University Press, Stanford, CA, USA: 428-438
West, L. 1986. Prey selection by individual snails. Ecology 67(3): 798-809
Table 1. Comparison of Relatve Abundance of frey and Ocenebra Diet Compostion
kedaive Abundane is mean area coveage ofa paticular prey rehive to mean tod area covered by prev¬
(Standard Deviation in parenthesis)
7 of Oenebra Diet is 9 of feding Oenebra which ae feding on a paricular prey tpe
Prey Item
% of Ocenebra
Relative Abundance
Diet
Tetraclita squamosa
59%
58% (4 81%)
Chthamalus spp.
26%
% (+ 48%)
Balanus glandula
3%
1% (+ 1%)
Macclintockia scabra
0%
4% (+ 10%)
Lottia paradigitalis
1%
1% (+ 1%)
Mytilus Californianus
3%
1% (+ 1%)
Phragmatopoma californica
1%
8% (+ 13%)
Other tube worm
8 1% (+ 1%)
3%
Table 2. Prey choice for 9snails marked in the Tetraclia and algae zones
2A. Sequence of prey choices. See legend below.
ailtt-///otl
snail 2i/-/o
Snail 3ittttrttt
snail ai-i
Snail sittt-ittssstlllttt
snail 6 —rt-//p- le
sail i/-Tsoerslen
Snail 8:/Ppp
tttssssog
Snail 9 ——-11-Tt-Tl
Legend: - : observed but not feeding
/no observation
T: feeding on Tetraclita
P: feeding on Phragmatopoma
C: feeding on Chthamalus
lowercase lettering, continuous feeding on the same prey individualas observed previousiy
25. Prey choiceby percent for same snais, fequeney of that pey in the det of the Ocenebra population
average in parenthesis under prey type.
Tetraclita Chihamalus Phragmatopoma
Total feeding
(59%
(26%)
(1%)
observations
Snail 1
100%
Snail 2
100%
Snail 3
100%
Snail 4
25%
Snail
100%
Snail 6
67%
33%
Snail 7
40%
60%
Snail 8
50%
50%
Snail 9
100%
Table 3. Fraction of times individuals were observed in each zone at low tide
3A. Snails initially observed and marked in Tetraclita and algae zones
Chthamalus zone
Tetraclita zone Algae zone
Total
0%)
(40%)
(40%)
observations
Snail 1
70%
30%
20
Snail 2
67%
33%
Snail
29
1Z
28%
18
Snail 4
829
18%
Snail 5
100%
18
Snail 6
100%
20
Snail 7
28%
72%
Snail 8
100%
Snail 9
6%
94%
17
FFrey types. T- Teraclita P- Phragmaiopoma Ce Chuhamdlus
3B. Snails initially obser ved and marked in Chthamalus zone
Chthamalus zone Tetraclita zone Total observations
(20%)
(40%)
Snail 10
100%
Snail 11
100%
Snail 12
100%
Snail 13
50%
50%
Snail 14
83%
17%
Prey
Types
T, I
T, P
T, C
T, P
lable 4. Prey choice for 7 snails in laboratory tanks.
4A. Sequence of prey choices. See legend below.
Snail 1:-SsC-s-Ss---C
Snail 2:T-TItttTtTt---
Snail 3:-TtttttIt/ttIttt-
Snail 4: —c--Tt
Snail 5:—-Ttttt-T-----Tt
Snail 6:—--T/-T-Itt-
Snail 7:—-Ss---M-
Legend: —: observed but not feeding
no observation
T: feeding on Tetraclita
C: feeding on Chthamalus
S: feeding on M. scabra
M: feeding on Mytilus
al. Prey choice by percent for samesnais relative abundance of hat prey in each tank in paenthesis
under prey type.
Tetraclita
Chihamalus Rytilus M. scabra L. paradigitalis
(64%)
(5%)
(19%)
(7%)
(6%)
Snail1
40%
60%
Snail 2
100%
Snail 3
100%
50%
Snail 4
50%
Snail 5
100%
Snail 6
100%
Snail 7
50%
50%
Total
feedings
FIGURE LEGEND:
Fig. 1. Snail locations within zones. Colored dots represent position of individual snails
at each low tide observation. Zones are shown in dashed lines, with corresponding zone
to the left.
Legend to colored dots. Snail umbers corespond with snails originaly marked in Feraclita and algae
zones, and represented in Tables 2 & 3
Snail 1:
Snail 2:
Snail
Snail 4:
Snail 5.
Snail 6:
Snail 7
Snail 8
Snail 9:
Fig.
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