Foraging Habitat of Sepia officinalis at STARESO Research Station in Calvi, Corsica,
France.
Colin Gaylord and Tyler Hubbell
ABSTRACT
The goal of our observational field study was to discover if the cryptic species
Sepia officinalis displays a habitat association while foraging at night. We predicted that
S. officinalis would show a strong preference for cobble and boulders covered in turfy
algae in the coves in and around STARESO research station. To test our hypothesis, we
compared the available habitat to where we located Sepia officinalis during night
sampling. Our study found that Sepia does show an association to at least the turfy algae.
This association is potentially due to Sepia officinalis’s mimetic abilities that may
enhance its foraging abilities and reduce the risk of predation.
INTRODUCTION
It is widely recognized that cephalopods represent the pinnacle of invertebrate
evolution. Animals in this class have adapted incredibly complex sensory systems and
have been shown to possess intelligence unrivaled among other invertebrates. A
centralized nervous system, including a relatively large, lobed brain found in numerous
cephalopods, allow for fined tuned interpretation and rapid response in regards to certain
environmental conditions (Boycott, 1961). This advanced centralized nervous system
provides the basis for several physiological characteristics that drastically increase the
likelihood of survival for many cephalopods. One of the most intriguing abilities in the
cephalopod class if found in Sepia officinalis, the common cuttlefish.
Cuttlefish are referred to by many as having the most highly adapted form of
camouflage in the animal kingdom. The skin of an adult specimen contains on the order
of 2 million pigmented chromatophore organs that are innervated to the brain (Hanlon &
Messenger, 1988). Dilation and contraction of the yellow, orange and brown
chromatophore organs allow for a widespread and nearly instantaneous change in body
color and patterning (Hanlon & Messenger, 1988; Hanlon & Messenger, 1996). Along
with chromatophore organs, Sepia possess’ reflecting iridiphores and light scattering
leucophores, which collectively allow for superior crypsis and signaling abilities
(Mäthger et. al, 2008).
The cryptic abilities of Sepia officinalis are well studied. It is accepted that,
though colorblind, cuttlefish visually cue in on their surroundings, particularly edges,
contrast, brightness, size etc., and use this information to adopt appropriate color and
textural patterns (Hanlon & Messenger, 1988, 1996; Mathger, et. al, 2006). It is
particularly interesting that even though cuttlefish do not perceive color, they effectively
display coloration that allows them to be cryptic with their surroundings. This is directly
attributable to the fact that the color variation between chromatophores, (orange, yellow
and dark brown) closely match that of the substrate (Mäthger et. al, 2008). Previous
papers have shown Sepia utilize three categories of camouflage patterns used in varying
substrates: uniform, mottle and disruptive. (Hanlon and Messenger, 1988; Hanlon 2007).
Substrate spatial scale is an important factor in informing which pattern a cuttlefish will
adopt.
Camouflage is the primary defense mechanism of numerous animals throughout
the animal kingdom. The complexity of the crypsis displayed by cuttlefish suggests the
immense selection pressure placed upon the organism by visual predators (Endler, 1986).
Not only do they alter their coloration, they often alter morphological characteristics to
more closely resemble their surroundings. These abilities offer two fold benefits for their
survival and proliferation. First off, they drastically decrease the likelihood of predation,
as predators simply will not see them. Secondly increased crypsis will make them more
efficient predators, expending less energy to catch prey as they can more effectively hunt
and ambush when they remain inconspicuous. With this in mind, it is evident that
cuttlefish crypsis and visual acuity of their predators have coevolved over time. As
cuttlefish are so finely attuned to their environment, it is reasonable to wonder if they
show specific habitat associations to certain substrates or primary placeholders. The
ornate displays of cuttlefish crypsis may allow them to be more or less vulnerable in
differing habitat, as in theory they can blend into some backgrounds better than others.
We attempt to show that cuttlefish do show habitat association in their natural
environment and offer explanations about why this might occur.
METHODS
General Approach
The goal of our study was to see whether Sepia officinalis associate to specific
habitat during foraging activities. In order to test our hypothesis, we conducted an
observational field study of Sepia officinalis. We characterized the habitat of the
surroundings of the research station, as well as where we found Sepia in the field.
Species Description
Sepia officinalis, otherwise known as the common cuttlefish, is found in the
waters of the Mediterranean to the eastern Atlantic from southern Norway to the
northwest coast of Africa as well as Madeira and the Canary islands (Khromov et al.
1998). They are a mobile species with greatest abundance found at depths of less than
100m. This species, like many other cephalopods, is primarily nocturnal but has been
observed during the day with some frequency. The common cuttlefish is usually found on
or close to the bottom and its morphology suggests adaptation to a complex environment.
It has been shown that cuttlefish visually cue on their surroundings in order to change
patterning to become more cryptic (J.J. Allen et al. 2010). Predation pressures are
suggested to have played a large role in their adaptation of textural, chromatic and
postural components of defensive strategies (Hanlon and Messenger 1996). Upon
observation, it becomes apparent that cuttlefish have the ability to rapidly change their
color and patterning using chromatophores. This is important to quickly and adaptively
respond to different habitats.
Site Description
We conducted our field study at STARESO Research Station Calvi, Corsica,
France (+42.580246, +8.72411). The marine environment around the station primarily
consists of Posidonia oceanica meadows and granitic bedrock reefs that extend off the
headlands. Surveys were performed to the North and South of the field station as well as
in the harbor of the station in order to characterize the largest amount of habitat available
for foraging.
The surveys we performed all took place October 9-30, 2012. Our habitat
characterization transects were run during the day, while our opportunistic sampling of
Sepia officinalis was conducted primarily at night.
Study Design (Specific Hypotheses)
Sepia officinalis associates to the shallow rocky subtidal environment while
hunting during the night. Specifically S. officinalis shows a preference to cobble and
boulder covered in turfy algal species. In order to show this we surveyed at night, which
is Sepia officinalis’s primary feeding, using a similar assessment of the habitat as used in
our UPC sampling but with S. officinalis individuals as our point contacts.
Data Collection
Surveys were conducted with another group to characterize available habitat in
and around STARESO harbor. Permanent transect lines were laid out in the harbor, in the
cove immediately south of the harbor and just to the north of the harbor. Non-fixed
transects were conducted perpendicularly off of these main transect line at intervals of 5
meters starting at the surface or as close to the surface as possible. Meter tape was run out
off the permanent transect line and depth was recorded at every meter. At every other
meter, uniform point contact was conducted with a 9 point quadrat to classify the
substrate composition as well as primary placeholders. These non fixed transect lines
extended either to the surface or to a length of 15 meters when it would be infeasible to
sample to the surface. Using this method, a profile of depth, substrate and primary
placeholders was established. Substrate was classified into distinct groups ranging from
sand, cobble, boulder, bedrock, concrete and jacks. As for primary placeholders a large
list of distinct categories of algae, sponges, encrusting species and Posidonia was
established. We decided to classify algae into 2 distinct groups, Turf and Bushy, based on
sizes less than 3 centimeters and greater than 3 centimeters respectively.
Opportunistic sampling was conducted on SCUBA primarily at night to assess
Sepia officinalis’ habitat association. These surveys consisted of meandering dives over
various substrate types from shallow subtidal depths to depths of 12 meters. When
individuals were found, they were sized, depth was recorded and a 9 point UPC quadrat
was employed to sample substrate and primary placeholder that the cuttlefish was found
over. Using this information, a clearer idea of available and utilized habitat will emerge
for the population of cuttlefish in the vicinity of STARESO.
For the statistical analysis of our data, the help of Pete Raimondi and his
knowledge of statistics was enlisted. With his help, our data was put into a
PERMANOVA table, which compared the average abundances of the available habitat
characteristics and the average abundance of sampled point of Sepia. This allowed the
data points of S. officinalis to be compared to the available habitat characteristics across
the 3 regions we sampled. Our dataset was separated into two tables: one being for
substrate and the other for the primary placeholders.
RESULTS
General Results
After analyzing our data, the results supported half of our initial hypothesis of the
habitat association of Sepia officinalis. Our prediction had two distinct features: one
being that S. officinalis associated with cobble and boulder substrates and that they also
associated with the Turfy algae types.
Primary Placeholder Results
The most conclusive evidence for the habitat associations of Sepia officinalis
comes from our data on the primary placeholders of our study site. As we predicted in
our hypothesis, Sepia show a disproportionate tendency to be found on the Turfy algae
type (Figure 1). We can say this with a high degree of certainty based of the p-value of
0.001, which is far below our critical p-value of 0.05 (Figure 2).
7
Average Abundances
6
5
4
Series1
3
Series2
2
1
0
T
B
POS
PD
Primary Placeholders
EL
Figure 1: Bar graph comparing the average abundances of the primary placeholders in the available
habitat (Red, Series 2) versus the average abundances of the primary placeholders that Sepia
officinalis (Blue, Series 1) was found on. Sepia was found disproportionately more frequently on
Turfy algae types. Average abundances are out of 9 total in reference to the 9 point UPC quadrats
that were used in sampling.
Primary placeholder
PERMANOVA table of results
Source
TR
Res
Total
Species
T
B
df
SS
MS
1
244
245
21646
6.66E+05
6.88E+05
Group
Cuttlefish
Av.Abund
6.36
1.43
Group Available
Av.Abund
2.58
3.77
21646
2730.2
Av.Diss
28.34
21.94
Pseudo-F
Unique
perms
P(perm)
7.9283
Diss/SD
0.001
999
39.99
30.96
Cum.%
39.99
70.95
Contrib%
1.51
1.15
POS
PD
EL
0
0.86
0.14
1.3
0.17
0.51
7.24
5.51
3.3
0.42
0.4
0.53
10.21
7.77
4.66
81.16
88.93
93.59
Figure 2: Table showing the average abundances of the available habitat and average abundances of
primary placeholders that Sepia officinalis was found on. Percent of contributions to the average
abundances are also shown, along with the p-value of this PERMANOVA table.
Substrate Results
Our results for the substrate habitat association of Sepia officinalis proved to be
inconclusive. The results showed that there were no strong associations to any substrate
type (Figure 2). Also, with a p-value of 0.055, which is above our critical p-value of 0.05,
there is not a significant amount of certainty in these particular results (Figure 4). Thus,
our hypothesis for the substrate association of Sepia is unsupported by our data.
4.5
Average Abundances
4
3.5
3
2.5
2
Series1
1.5
Series2
1
0.5
0
BO
BD
CO
SA
Substrate
Figure 3: Bar graphs showing the average abundances of the available substrate types in the study
site (Red, Series 2) versus the average abundances of substrate types that Sepia officinalis was found
on (Blue, Series 1). Average abundances are out of 9 total in reference to the 9 point UPC quadrats
that were used in sampling.
Substrate
PERMANOVA table of results
Source
df
TR
1
Res
511
Total
512
Groups Cuttlefish & Available
Average dissimilarity = 74.63
Group Cuttlefish
Species
Av.Abund
BO
3.21
BD
3
CO
2.14
SS
MS
7426.9
1.66E+06
1.66E+06
Group Available
Av.Abund
3.96
0.71
1.38
7426.9
3241.1
Av.Diss
24.09
18.73
15.33
Pseudo-F
2.2914
P(perm)
0.055
Diss/SD
Contrib%
32.28
25.1
20.54
1.14
0.76
0.89
Unique
perms
996
Cum.%
32.28
57.38
77.92
SA
0.64
1.66
11.67
0.56
15.63
93.55
Figure 4: Table showing the average abundances of the available habitat and average abundances of
substrates that Sepia officinalis was found on. Percent of contributions to the average abundances are
also shown, along with the p-value of this PERMANOVA table.
DISCUSSION
The substrate portion of our results proved to be the least significant and did not
support our specific hypothesis for Sepia. There are a couple potential reasons as to why
we did not get the results we were predicting. The first issue comes from our sample size
and the comparison of the habitat data to the data on Sepia. Essentially we were trying to
compare around 900 habitat quadrats to 14 quadrats for Sepia officinalis. Ideally we
would have had more samples for Sepia; however, attempting to study a less common
cryptic species yielded a much smaller dataset than we were expecting. The next issue
may have come from how we decided to sample with the quadrat. We were taking 9
points of data for substrate for each individual Sepia, this may have led to an over
representation of the surrounding habitat as opposed to what the cuttlefish was actually
located on.
As we predicted, Sepia officinalis showed an association to the Turfy algae
species of the primary placeholders we surveyed. This result makes sense for reasons that
we mentioned in the introduction. Sepia’s cryptic abilities have distinct characteristics
and limitations. Their ability to mimic texture in the three dimensional habitat is limited
by the extent their musculature can shift. Thus it makes sense that Sepia officinalis
associate to the Turfy algae, which it can mimic best based on, “the animal’s texture
perception” (Kelman et al. 2007).
Our study showed that Sepia officinalis does associate to a particular habitat while
foraging at night. Potential reasoning behind this association may have to do with the
ability of Sepia to mimic its environment in color and, to a degree, in its form. As we
mentioned earlier, there are a number of benefits to remaining cryptic while foraging.
First of all, it could allow Sepia to be a more effective ambush predator and expend less
energy while hunting. Second, having exceptional camouflage, “thwarts a wide array of
visual predators” (Mäthger et al 2008).
Many studies have been performed to study the disruptive body patterns and
matching of natural substrates (Kelman et al 2007, Mäthger et al 2008). These studies
have shown that Sepia do in fact have the extraordinary ability to mimic their
environment, and with our study we aimed to answer how they use this trait in their
habitat. By showing that Sepia officinalis do prefer a certain aspect of their environment
while foraging, the door is left open to a whole host of other questions regarding Sepia’s
interaction with its environment. Future studies could attempt to follow up on our
question by analyzing Sepia officinalis’s preferred environment for potential prey items
or hiding locations.
Studying a predatory species such as Sepia officinalis is very important because
so little is truly known about their role in the ecosystem. It is unknown the level of impact
these predators have on their environment, but the first step to understanding this
question is to find our where they happen to be found.
LITERATURE CITED
Allen, J.J., et al. 2010. Cuttlefish dynamic camouflage: responses to substrate choice and
integration of multiple visual cues. Proceedings of the Royal Society of London B. 277.
1031-1039.
Boycott, B., 1961. The Functional Organization of the Brain of the Cuttlefish Sepia
officinalis. Proceedings of the Royal Society of London. Series B, Biological Sciences,
Vol 153, No. 953: 503-534
Endler, J.A. 1986. Natural Selection in the Wild. Monographs in Population Biology 21.
Princeton University Press. 336pp.
Hanlon, R.T. ,2007. Cephalopod dynamic camouflage. Current Biology 17(11): R400R404
Hanlon, R.T. , J.B. Messenger. 1988. Adaptive Coloration in Young Cuttlefish (Sepia
officinalis L.): The Morphology and Development of Body Patterns and Their Relation to
Behavior. Philosophical Transactions of the Royal Society of London. Series B,
Biological Sciences, Vol. 320, No. 1200: 437-487
Hanlon, R.T., J.B. Messenger. 1996. Cephalopod behavior. Cambridge University Press
Kelman, E.J., A.J. Shohet, D. Osorio, R.J. Baddley. 2007. Perception of visual texture
and the expression of disruptive camouflage by the cuttlefish, Sepia officinalis.
Proceedings of the Royal Society B. 274. 1369-1375 .
Khromov, D.N., Lu, C.C., Guerra, A., Dong, Z. & Boletzky, S.V., 1998. A synopsis of
Sepiidae outside Australian waters (Cephalopoda: Sepioidea). In Systematics and
biogeography of cephalopod, vol. I (ed. N.A. Voss et al.). pp.77^57. Smithsonian
Contributions to Zoology, no. 586.
Mäthger et al., 2006. Color blindness and contrast perception in cuttlefish (Sepia
officinalis) determined by visual sensorimotor assay. Vision Research, 46(11): 1746-1753
Mäthger et al., 2008. Color matching on natural substrates in cuttlefish, Sepia officinalis.
Journal of Comparative Physiology, 194: 577-585
APPENDIX
It should be noted that our project did not turn out exactly how we planned.
Initially we intended to have both laboratory and field portions of our study. With
numerous studies showing that substrate composition affects cuttlefish patterning and
behavior, we wanted to examine if this patterning is context specific. We planned on
examining cuttlefish behavior and patterning over varying substrates and how it changed
in response to varying stimuli (i.e. predators, prey, other cuttlefish). We planned on
taking video of our trials and analyzing the chromatophoric pattern shifts over different
parts of the body and quantifying them by scoring the type of display seen. Several
cuttlefish were captured over the course of our trip and housed individually in a roughly
35cm^3 clear aquarium. Cuttlefish were fed triple fin and blennies to establish a prey
preference to use in the study. Because feeding the cuttlefish every trial seemed infeasible
for our design, we put the triple fin in a 5cm long clear glass cylinder and attached fishing
wire to drop it into the tank to attain replicates. Because the cuttlefish were very
responsive to triple fin outside the jar, quickly capturing and consuming the prey, we
figured they would do the same at least a few times with the contained prey item.
However, we never witnessed one response from the test subjects even though dozens of
trials were run.
We ran into similar problems testing response to predators. This design consisted
of placing a 35cm^3 tank adjacent to the cuttlefish tank and adding an octopus much
larger than the cuttlefish. Again, no response was measured. A blind was added to try and
attain replicates in this test.
Sadly, we ran into problems trying to keep our specimens alive over the duration
of our stay. Francis, the first cuttlefish we caught lived in the tank for nearly a week
before tragically passing away. However, in this unfortunate event we were able to
capture a definitive cuttlefish stress response of two black dots on the dorsal posterior of
the mantle. We thought this display was attributable to adding a larger than prey size fish
to the tank, however it probably was also effected by the vulnerable, weak state of
Francis.
During the course of our project we learned quite a bit, primarily that cuttlefish
are hard to maintain in a lab setting. They are very sensitive creatures that need a lot of
space. They are also have a voracious appetite and can become cannibalistic if left in
close quarters with other cuttlefish without enough food. In the field they are easiest seen
and captured at night over turfy algae. In the laboratory setting, more, larger tanks, closed
off from the stimulus of in the room would have aided in our ability to successfully
maintain the specimens. We could have benefited from more time to figure out how to
work with the animals. All in all, we were lucky we had a field portion of our project to
fall back on. A contingency plan is a good idea when working with a less common,
unpredictable cryptic species.
Acknowledgements
Thank you Pete, Giacomo, Kristen, Jimmy, and Gary. This class was an amazing, eye
opening learning experience. Thank you for sharing it with us.