Comparison of prey utilization in the lab and field
for Octopus vulgaris
Caitlin Carrington, Khanhchi Dam, Nicole Magana, and Ian Roussopoulos, 2012
Abstract:
The relationship between prey utilization in the lab and field was investigated for
Octopus vulgaris individuals in Calvi, Corsica, France. Midden contents were collected from 21
dens surveyed near STARESO research station. Nine of the occupants of those surveyed dens
were captured and subjected to preference trials in the lab. Prey selection in the field was found
to be significant and could be grouped geographically. O. vulgaris individuals showed
statistically significant preference behavior during lab trials. Utilization in the field and lab,
however, did not mirror each other, supporting that O. vulgaris act as opportunistic generalists in
the field, but specialists in the lab.
Introduction:
Optimal foraging theory states organisms minimize energy spent in prey capture (search
time) and consumption (handling time) while also minimizing personal risk and maximizing
caloric intake. Generalist predators achieve this by feeding opportunistically from multiple
available prey items. Specialists achieve optimal foraging by reducing handling or search time
through the particular specialization they have evolved to capture and consume their prey. Being
a generalist predator has the advantage of allowing the organism to survive through
environmental conditions that may reduce the diversity of prey available to it at a given time.
Conversely, specialist predators have the advantage of more quickly and efficiently capturing
prey than their generalist counterparts making them more effective predators when their
particular prey type is available (McPeek 1996).
Octopus vulgaris has been shown to be an extremely intelligent animal that is adept at
problem solving (Hamilton 1997). This high level of intelligence makes them especially good
hunters, and allows them to successfully capture a wide variety of prey (Ambrose and Nelson
1983). O. vulgaris is considered a generalist predator, but work has been done that shows
individuals may specialize on particular prey items (Anderson et al 2008). This is interesting
because generalist species tend not to include individuals who specialize in specific prey
selection, and specialists tend not to be capable of utilizing a wide variety of prey. Other animals
that exhibit this behavior, such as dolphins and primates, are highly intelligent and capable of
capturing a wide variety of prey, but can also adapt intellectually to fill environmental niches
(Meynier 2008, Chapman and Chapman 1999). To have an invertebrate animal showing similar
behavioral patterns as these highly intelligent vertebrates is unique, and warrants investigation.
To our knowledge, no study has been done that directly compares data on prey utilization
by O. vulgaris in the field with prey preference lab experiments done on those same individuals.
We investigated the foraging behavior of O. vulgaris through midden collections done in the
field at the STARESO research station. We also used lab based experiments of prey choice to
determine the level of diet preference that is statistically significant in O. vulgaris. By running
prey preference experiments and comparing the results with midden compositions, we hope to
more clearly show whether these animals are opportunistic predators, strictly generalists,
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specialists, or show individual behavioral preference when it comes to selecting their prey.
Specifically, we have three questions and predictions we are interested in addressing:
1) Does prey selection in the field vary geographically?
We predict that individuals residing in close proximity with each other will exhibit
more similar prey utilization than those from groups of individuals who are separated
geographically.
2) Do Octopus vulgaris individuals exhibit prey preference?
We predict that we will see a significant pattern among O.vulgaris individuals who
are offered a choice in available prey, specifically that a particular prey item will be
chosen more often than any other.
3) Will the prey preference shown in the lab be reflected in individuals from the field
locations surveyed?
We predict that one of the three prey items offered in the lab experiments will be
consistently chosen regardless of the prey selection shown by that individual in the
field.
If our predictions are correct they will support the hypothesis that these animals may act as
opportunistic generalists in the wild, but show preference in selecting prey when confounding
factors such as prey availability and risk of predation are removed.
Methods:
Study Site
This study was conducted at STARESO Research Institute of Oceanography (42° 34’ N,
08° 43’ E) near Calvi, Corsica during October 2012. STARESO’s harbor is bordered by granite
cliffs on the South and a jetty on the North. The South side offers a shallow rocky-to-sandy
bottom, while the North side offers a slightly deeper, rocky substrate. North of the harbor the
substrate is composed largely of granite boulders and cobble, while the South is characterized by
many coves containing smaller rocks.
Species Description
The common octopus, Octopus vulgaris, is frequently used in laboratory studies. It is
distributed throughout the tropical and semitropical waters of the world (Wood & Day 1998).
This includes the Mediterranean Sea and the waters off of Corsica where this study was
conducted. O. vulgaris lives a benthic life from very shallow water to a depth of 200m, and lives
for 1-1.5 years (Wood & Day 1998). From arm to arm they can reach anywhere from 1 to 3 feet
(Octopus vulgaris 1999). They commonly predate upon gastropods and bivalves at dusk, which
has been confirmed both in the lab and by studying them in their natural habitat (Octopus
vulgaris 1999). To kill and consume their prey, O. vulgaris can either pull the prey’s shells apart,
or drill into it with their radula (McQuade 1993). They are quite often difficult to spot because of
their remarkable ability to camouflage. However, they have conspicuous dens underneath
boulders or in cobble that are surrounded by “middens”, or the discarded shells or exoskeletons
of their prey (Wood & Day 1998). These middens are commonly studied to examine not only
what the octopus is consuming, but also to determine which prey species are present in that area
(Wood & Day 1998).
Field Methods
Snorkeling and SCUBA surveys were done from 150m north of the harbor mouth to 70m
south to find possible O. vulgaris dens. Candidate dens were given a random number from 1
through 30 and tagged with flagging tape (Figure 1). Once dens were located and tagged, surveys
were done every 1-4 days over a two week period to collect midden piles and record den
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occupancy. Shells were collected within a 1m radius of each den. Surveys began with seven
dens, and dens were added to the study for the first week until the final sample size of 21 dens
was reached. The depth, GPS coordinates, and den composition was recorded for each site.
Midden contents were counted, categorized into groups by prey type, and measured to the
nearest millimeter along the longest axis using calipers. Where possible, bivalve shells were
matched, and unmatched shells counted as single individuals, a method which is commonly used
in midden studies (Mather 1991a). Shells were grouped by type as follows: abalone, Arca, clam,
crab, limpet, Mytilus, other, oyster, scallop, and snail. Shells that could not be identified were
grouped into other.
Lab Methods
Octopuses were captured throughout the study for lab trials. Individuals were caught at
marked dens so midden data could be compared to lab results. A total of nine octopuses were
caught from depths between 5 and 20 feet by SCUBA and skin divers who used a combination of
aquarium nets and goody bags to coax each octopus from its den. Individuals were kept in one of
three aquariums (tank 1: 100x50x50cm, tank 2: 60x70x127cm, and tank 3: 44x38x44cm) for a
period of 3 to 5 days. No octopus was ever kept in the presence of another to reduce stress,
aggression, and competition. Before release, five successful prey preference trials were
conducted. A successful trial was defined as one in which the octopus consumed at least one of
the prey options. Each octopus was presented with three prey options: mussel (Mytilus
galloprovincialis), Arca noae, and abalone (Haliotis lammelosa). Abalone and Arca were chosen
because they appeared in study middens at a high frequency, and because they were easily
collected in the STARESO harbor by skin divers. Mytilus was found at a lower frequency and
was chosen to act as the novel option. Using calipers, the length of each prey item was measured
(mm) along the longest axis. The time of day and duration of the trials were recorded by
stopwatch. Trials were run at dawn, dusk, and night due to the octopus’ inactivity during the
majority of daylight hours. After the prey items were placed in random order equidistant from
each other on one or the other side of the aquarium, the octopus’ choice was observed and
behavior recorded for a maximum of fifteen minutes. The two prey items not chosen were
removed either once the octopus began to consume its prey or once the trial was terminated
depending on which would cause less disturbance to that individual. Prey items not chosen were
placed in a holding tank with flow through seawater. If the octopus did not consume anything or
made no movements within the allowed fifteen minutes, all three prey items were removed. The
octopus was given a minimum of one hour in between trials to increase the motivation to eat.
Before release, 6 octopuses were tagged by injecting a unique color of latex paint under the skin
either on the mantle or between two of the arms. Subcutaneous latex paint tagging has been
proven to have high visibility and retention rates, as well as cause minimal damage and mortality
in fish (Wolfe and Marsden 1998). All octopuses were released within 2-10 meters of the den
they were captured in when weather conditions allowed. Experimental tanks were emptied and
cleaned between octopuses to prevent the next inhabitant from chemosensing the previous
octopus or mucous trails from previous prey items. Octopuses which were recaptured less than
24 hours after release were released again, but 2 individuals were caught more than 24 hours
after release and held for an additional 5 trials in the lab.
Statistical Analysis
In order to determine if dens could be grouped geographically by midden contents, the
number of shells corresponding to each prey category was tallied for each den. The total number
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of shells found for each den on each sampling day was also tallied to determine good sampling
days for each den. A good sampling day was considered a day where at least 5 shells were found
at that den. Data from all other sampling days was dropped. Additionally, dens were omitted if
the total number of shells found at that den throughout the entire study totaled less than 10 shells.
A PERMANOVA test was run to determine the overall p-value for the relationships between
midden contents at each den. The critical p-value for all tests was set at p=0.05. The
PERMANOVA test included a pairwise comparison of each geographic group and gave a pvalue for each pair. Dens were grouped by geographical location as residing north of the harbor
mouth (N), south of the harbor mouth (S), the north half of the harbor (NH), or the south half of
the harbor (SH). North and south harbor were delineated by a line which began at the ladder in
the STARESO dock (42°34'48.85"N, 8°43'26.84"E) and ran at a heading of 150° to the harbor
mouth. A transect line was put in place at the beginning of the study and left until the last
sampling day. A SIMPER test was also run to evaluate prey type abundances and their
contributions to the differences between each pair of den groups. A Bray-Curtis cluster analysis
was done to determine the level of dissimilarity between each of the dens.
Figure 1: Diagram of the den numbers used in statistical analysis and locations in and around the harbor at
STARESO. The area north of the harbor mouth is labeled “N,” the area south is labeled “S,” and “H” denotes the
harbor.
To determine if preference was exhibited in the lab, data on selected prey, position of
prey in tank, and size of all prey were recorded and analyzed using Analysis of Similarity
(ANOSIM) which gave a pairwise comparison to detect differences between groups of prey
preference. A Bray-Curtis cluster analysis was done to show the level of dissimilarity between
groups.
To compare the prey selection in the field to preference in the lab, we only included field
data that was used in the statistical methods previously described. We also included only those
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lab subjects that were captured from the analyzed dens. Both sets of data were formatted so they
could be directly compared using a RELATE test.
Results:
A Bray-Curtis cluster analysis on our field midden data showed dens could be grouped
geographically (Figure 2). North harbor (NH) and South (S) were the most similar, and north (N)
was the least similar to the other groups. In light of this result, all other tests were run with
respect to geographic group. The PERMANOVA test gave a p-value of 0.001 for the overall test
and significant p-values for three out of the six pairwise comparisons (Table 1). The SIMPER
analysis showed Arca and abalone as the top two prey types contributing to the dissimilarity
between groups of dens, by as much as 50% and 45% respectively, except for the comparison
between the S and SH groups where crab and abalone were the top two contributors (Table 2).
Group average
Transform: Square root
Resemblance: S17 Bray Curtis similarity
50
Distance
40
30
20
S
NH
SH
0
N
10
Samples
Figure 2: Bray-Curtis cluster analysis. The closer the horizontal lines are to the x-axis, the more similar the
connecting groups are.
Table 1: The PERMANOVA analysis shows significant differences between the dens in each geographic region. Pvalues are given under the P(perm) headings. The lower portion shows p-values for each pair of regions.
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Table 2: SIMPER analysis of four geographic pairings. Prey types in each group were compiled into average
abundances and compared, and the percent contributions were determined. Contributors were ranked from highest to
lowest for each pair.
We ran an ANOSIM test to answer our second hypothesis about prey preference in the
lab. It showed that captured octopuses significantly demonstrated a prey preference in our
laboratory setting (p=0.001) (Table 3). All captured octopuses selected abalone during at least
two out of five successful trials. The Bray-Curtis cluster analysis divides eleven sets of trial into
three subgroups (a, b, and c) according to the similarity of their prey selections (Figure 3). Group
a, consisting of three individuals, only ate abalone. Group b selected abalone four out of five
trials. Group c chose only two or three abalone during their trials. Both groups a and b showed a
strong preference for abalone compared to group c. In Figure 4, individuals from group a and b
are scattered around the vector associated with abalone, while individuals from group c cluster
around either Mytilus or Arca. Out of 55 trials, Arca was only chosen once.
Table 3: An ANOSIM test shows a statistical comparison of prey selection for captured octopuses and yields a pvalue 0.001.
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Group average
Resemblance: S17 Bray Curtis similarity
50
Group
b
c
a
Similarity
60
70
80
90
The Kraken
Little Ian
Chubs
Cedric
Little Jimmy
Cedric
Littlest Khanchi
Tiger
Little Caitlin
Chuck Norris
Little Caitlin
100
Samples
Figure 3: Bray-Curtis Cluster analysis of prey selection for octopuses in the laboratory. The X-axis represents
individual octopus IDs, and the Y-axis shows a scale of similarity.
Resemblance: S17 Bray Curtis similarity
2D Stress: 0
Group
b
c
a
The Kraken
Arc
Chuck Norris
Cedric
Littlest Khanchi
Ab
Myt
Chubs
Little
Caitlin
LittleTiger
Caitlin
Cedric
Little Ian
Little Jimmy
Figure 4: Bray-Curtis cluster analysis of prey selection for octopuses in the laboratory. The three vectors dividing
the diagram signify the three types of prey.
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The RELATE test was used to analyze our third hypothesis, and the Spearman Rank
Correlation analysis yielded a significance level of 50.3%. Thus, the prey utilization in the field
was significantly different from the prey preference exhibited in the lab.
Discussion:
The results from the field portion of our study made it clear that our subjects’ diets varied
by region. The geographic groupings we chose during our sampling were both for convenience
and because the habitat appeared to vary between regions. The south (S) and north harbor (NH)
regions were characterized by small cobble and rocks (< 10cm) and dark-colored turf algae. The
south harbor (SH) region was mostly composed of fist- to boulder-sized rocks (>10cm to 2m)
and light-colored bushy algae. The north (N) region had highly variable substrate, and although
the algae appeared similar to the SH region, it was patchy and less dense. It is reasonable to
predict that such variable habitats might yield similarly variable densities and/or availability of
prey types. We expect this to be a likely explanation for the differences we observed in midden
composition, though our study did not include surveys or estimates of prey presence in these
regions. Another likely cause could be individual preference. However, as we will discuss later,
our lab results ruled out that possibility for this group of individuals.
It is not surprising that our SIMPER test revealed abalone and Arca as the top two
contributors in the differences in prey selection between most of our regions. As we collected
middens, we noticed that most were primarily composed of either Arca or abalone, with few
exceptions (one of the dens in the NH region heavily favored scallops, and another two in the
same region always had crabs in their middens). It was rare that a midden pile would contain
comparable quantities of both Arca and abalone, which provides more evidence that prey
availability in each area might be variable.
For the lab experiment, all captured octopuses showed a strong preference for abalone.
Possible explanations might include the difference in caloric content and handling time among
the three prey types offered. We noticed that the Arca used were much smaller in size compared
to the other two prey items offered as well as what we found in the middens. Therefore, Arca
might offer a lower nutritional value. Additionally, abalones seemed to be easier to handle
because they are not enclosed in two shells like the bivalves. This might be another factor that
explains abalone popularity among our lab subjects. Controlling for variables like size and
caloric content of the prey could give a more definitive conclusion.
Our study shows strong supporting evidence for the idea that Octopus vulgaris
individuals act as opportunistic generalists in the field, but show preference in prey selection
when confounding factors such as risk of predation and prey availability are removed, such as in
the lab. Our results demonstrate that there was absolutely no relationship between what our study
octopuses were choosing in the lab versus in the field. This is consistent with a key assumption
of optimal foraging theory, which states that individuals will try to lower their risk of predation
in lieu of pursuing preferred prey. Common predators of octopuses in the Mediterranean are
moray eels and conger eels (Common Octopus 2010), which we observed to be prevalent in our
study area. Thus, it is more beneficial for an individual to hunt within its home range, where it
can easily navigate back to the protection of its den, regardless of whether its preferred prey is
found within that range. This will lead to the octopuses not always consuming their preferred
prey type, but instead selecting prey based on factors such as availability.
An additional observation noted in the lab was a hoarding-like behavior displayed
occasionally by some individuals. This would occur most frequently with recaptured individuals,
or those who were nearing the end of their five trials. An individual would first select a prey item
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with one arm, then grab the remaining prey items and tuck them under its mantle. This behavior
prevented us from removing the remaining prey items as per our experimental procedure. This is
compelling as it appears the animals were learning the pattern of the experiment and
remembering that items were being taken away at the end of each trial. This suggests that they
made an association between selecting a prey item and the subsequent removal of the remaining
prey items. This may reflect behavior in the field when an octopus individual is attempting to
hunt in the presence of other predators or competitors.
Though O. vulgaris is a well-studied species, there is still much to learn. One possible
direction for future research would be to examine the strength of the correlation between midden
composition and prey availability. This would be accomplished through invertebrate transects
carried out in areas that encompassed the home ranges of octopuses and comparing that data to
the midden compositions of those individuals. This sort of study would be useful for
investigating the distance octopuses travel to hunt in this area of the Mediterranean, as well as
how the surrounding area’s invertebrate composition influences prey selection. One study
claimed the hunting grounds of O. vulgaris to extend as much as 100m from the den (Mather
1991b). None of the dens in our study were more than 80m away from its nearest neighbor, and
many were less than 10m apart. If the hunting ranges of the octopuses in our study were
overlapping, we would expect their midden compositions to be much more similar. However,
prey availability cannot be verified without further study. By knowing exactly how much of each
prey type is available we would be able to more confidently estimate the distances these
octopuses travelled to retrieve prey and the degree of prey specialization present between
octopus individuals.
Our study was unable to include all possible prey types found in the middens at
STARESO and the surrounding areas. To address this, surveys of midden composition could be
done again, and trials of similar experiments could be run in the lab but using all the prey types
found during the midden surveys, as well as one or two completely novel options. It would be
informative to create a hierarchy of preferred food, and compare it among individuals to see
what, if any, intraspecies diet similarities exist. For this, researchers should do a bomb
calorimetry test on all prey types to see how the calorie content of the prey varies between size
and species. Through this, we can see if the octopuses prefer prey based on calorie content, or if
there are other factors controlling prey preference in the lab such as handling time or previous
experience.
Lastly, we propose a further study to document changes in midden composition over
time. Over an individual’s lifetime, this may show the learning process in prey selection, or
seasonal differences in prey usage. Learning the patterns associated with octopus prey selection
would allow us to more effectively administer a conservation effort on their behalf should it
become necessary. Paring midden compositions with data on changing environmental factors,
such as water temperature, over several octopus generations could shed light on the versatility of
this species’ diet and predatory behavior under stress. As a model species of specializing
generalist predators, this may also set standards for other organisms similarly affected by
environmental change.
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Acknowledgements:
We would like to sincerely thank Pete Raimondi, Giacomo Bernardi, Jimmy O’Donnell,
Gary Longo, and Kristin de Nesnera for their help and guidance throughout our research. We
would also like to thank the Marine Ecology Field Quarter class of 2012 for their help in locating
and capturing octopuses and collecting middens. Finally, merci beaucoup to the staff at
STARESO Research Institute of Oceanography for housing our research effort.
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