Animal Cognition

https://doi.org/10.1007/s10071-018-1209-8

ORIGINAL PAPER

Variability in the “stereotyped” prey capture sequence of male

cuttlefish (Sepia officinalis) could relate to personality differences
Francesca Zoratto1   · Giulia Cordeschi1 · Giacomo Grignani2 · Roberto Bonanni3 · Enrico Alleva1 ·
Giuseppe Nascetti2 · Jennifer A. Mather4 · Claudio Carere2,5

Received: 8 August 2017 / Revised: 17 August 2018 / Accepted: 23 August 2018

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract
Studies of animal personality have shown consistent between-individual variation in behaviour in many social and non-social
contexts, but hunting behaviour has been overlooked. Prey capture sequences, especially in invertebrates, are supposed to be
quite invariant. In cuttlefish, the attack includes three components: attention, positioning, and seizure. The previous studies
indicated some variability in these components and we quantified it under the hypothesis that it could relate to personality
differences. We, therefore, analysed predation sequences of adult cuttlefish to test their association with personality traits in
different contexts. Nineteen subjects were first exposed to an “alert” and a “threat” test and then given a live prey, for 10 days.
Predation sequences were scored for components of the attack, locomotor and postural elements, body patterns, and number
of successful tentacle ejections (i.e. seizure). PCA analysis of predatory patterns identified three dimensions accounting
for 53.1%, 15.9%, and 9.6% of the variance and discriminating individuals based on “speed in catching prey”, “duration of
attack behaviour”, and “attention to prey”. Predation rate, success rate, and hunting time were significantly correlated with
the first, second, and third PCA factors, respectively. Significant correlations between capture patterns and responsiveness
in the alert and threat tests were found, highlighting a consistency of prey capture patterns with measures of personality in
other contexts. Personality may permeate even those behaviour patterns that appear relatively invariant.

Keywords  Cephalopods · Hunting behaviour · Animal personality · Behavioural consistency · Welfare

Introduction

Until recently, predatory behaviour of cephalopods was

Electronic supplementary material  The online version of this
article (https​://doi.org/10.1007/s1007​1-018-1209-8) contains
supplementary material, which is available to authorized users.
* Francesca Zoratto
francesca.zoratto@iss.it
1
Centre for Behavioural Sciences and Mental Health, Istituto
Superiore di Sanità, Viale Regina Elena 299, 00161 Rome,
Italy
2
Ichthyogenic Experimental Marine Centre (CISMAR),
Department of Ecological and Biological Sciences,
University of Tuscia, Tarquinia, Viterbo, Italy
3
Independent Researcher, Via Giuseppe Donati 32,
00159 Rome, Italy
4
Department of Psychology, University of Lethbridge,
Lethbridge, Canada
5
Laboratory of Experimental and Comparative Ethology,
University of Paris 13, Sorbonne Paris Cité, Villetaneuse,
France
generally supposed to be fairly fixed, as it is thought hav-
ing a strong stereotypic sequence pattern; as a consequence,
variability in the predatory behaviour has been largely over-
looked. However, recent studies do show to some extent
individual differences in predatory behaviour. The motor
pattern of movement of cephalopod muscular hydrostat
systems has been studied in detail with analysis of octopus
arm reaching (Flash and Hochner 2005), but the patterns of
more fixed sequences have mostly been ignored. Especially,
with cephalopod behaviour being so variable, fairly fixed
sequences could get simply catalogued (e.g., sand-digging
behaviour; Mather 1986; Anderson et al. 2004). This is the
case of the predatory behaviour of cuttlefish (Sepia offici-
nalis, Linnaeus 1758), which was first supposed to be quite
invariant (e.g. Wilson 1946) and thus even classified as fixed
action pattern (FAP; Bonner 1980). The latter is defined as
a complex motor act involving a specific temporal sequence

13
Vol.:(0123456789)

of unlearned repetitive movements, which is triggered by an
external stimulus and is influenced by underlying motivation
but relatively unaffected by feedback (Lorenz and Tinbergen
1938; Dixon et al. 2008).
When classical work is screened in detail, some varia-
tion in many components is revealed (e.g. Messenger 1968;
Duval et al. 1984). Indeed, such sequences are also named
modal action patterns (MAP), a term that considers indi-
vidual variation in performance by referring to the mode (i.e.
the most frequent measurement value) shown in the distribu-
tion of the behavioural pattern (Barlow 1968; Dixon et al.
2008). For example, grooming in mice contains specific
repetitions of head, arm and paw movements, classifiable in
four distinct phases, which, once started, will continue even
if feedback from physical contact with the body is prevented
(Berridge 1990).
Accordingly, most authors do not make reference to FAPs
in cephalopods (e.g. Mather 2011). Mather (1986) showed
that sand-digging behaviour is accomplished by both stereo-
typed and variable components, which suggests that a FAP is
exhibited as an “open programme” to adjust it on the basis of
sensorial feedbacks (e.g., inspection of the substrate). This
behaviour has some internal flexibility: the general sequence
of discrete acts remains fixed, but the micro-sequences are
somewhat variable and the durations change with different
contexts (Mather 1986). Therefore, it better fits the definition
of modal action patterns, sensu Barlow (1977).
In the past two decades, many researchers have reported
consistent individual differences in behaviour across differ-
ent contexts, even in species less considered (like inverte-
brates), and have hypothesised that such a variation could be
partly attributed to personality differences (see Carere and
Eens 2005; Carere and Maestripieri 2013). These studies
have evidenced that in a large variety of non-human spe-
cies consistent individual differences in one trait covary with
other behavioural and physiological traits. Behaviours that
are organised in such a way are denoted as behavioural syn-
dromes, that is, suites of correlated behaviours reflecting
between-individual consistency across different situations
(Gosling 2001; Sih et al. 2004; Groothuis and Carere 2005;
Reale et al. 2007).
Recent studies in cephalopods (only one on cuttlefish)
have found consistent behavioural differences (over time,
situations, and/or contexts) using a “bottom-up approach”,
i.e., testing animals in common situations and analysing
their behaviour with multivariate statistical methods with-
out a priori expectations, to detect patterns of covariation of
variables that may correspond to personality axes. In par-
ticular, the principal component analysis (PCA) is a multi-
variate statistical approach (Giuliani et al. 1994, 2004) suc-
cessfully employed to investigate personality in several taxa
(e.g. Mather and Anderson 1993; Natoli et al. 2005; Ferrari
et al. 2013). In red octopus (Octopus rubescens; Mather and
13
Animal Cognition
Anderson 1993), two-spot octopus (Octopus bimaculoides;
Sinn et al. 2001), gloomy octopus (Octopus tetricus; Pronk
et al. 2010), dumpling squid (Euprymna tasmanica; Sinn
and Moltschaniwskyji 2005), and cuttlefish (Sepia offici-
nalis; Carere et al. 2015) a set of personality axes (i.e. factors
of the PCA; see the “Methods” for a detailed explanation of
how the procedure works) emerged similar to those found
in vertebrates, with three or four axes accounting for a range
from 45 to 78% of the total variance (see Mather and Logue
2013 for invertebrates; see Gosling 2001 for a comparison
with vertebrates).
Cuttlefish are active generalist predators, able to catch
comparatively large living prey (Hanlon and Messenger
1996; Guerra 2006). Is there any substantial individual var-
iation in their predatory behaviour? Various accounts are
available since the first description of the attack on prawns
by Sanders and Young (1940) (e.g. Holmes 1940; Wilson
1946; Boycott 1958; Messenger 1968; Duval et al. 1984;
Adamo et al. 2006). In each “attack” (i.e. an attempt to seize
a prey during a “hunting sequence”), it is possible to rec-
ognize three consecutive components, termed “attention”,
“positioning”, and “seizure” (e.g. Sanders and Young 1940;
Messenger 1968).
During “attention”, the cuttlefish aligns itself with the
prey. Attention behaviour may vary between 1 and 10 s in
duration according to Messenger (1968), but last up to 120 s
according to Duval et al. (1984). During “positioning”, the
cuttlefish moves until it is about one mantle length from its
prey. Positioning behaviour may be over in less than 1 s or
may last for more than 10 s. “Seizure”, the final component,
can be accomplished by two distinct methods of attack (Mes-
senger 1968; Duval et al. 1984): (1) the “arm grab”, mainly
used on crabs (depending on crab size and other factors),
involves the use of all the arms without the tentacles once
the animal has jumped upon its prey and (2) the “tentacle
strike”, used on rapidly escaping preys like shrimps and fish,
involves the ejection of the prehensile tentacles, which are
rapidly shot out towards the prey and then retracted to bring
the prey to the arms and the mouth. The “arm grab” (dura-
tion 200–1000 ms) is slower than the “tentacle strike” and
it allows the use of visual feedback, which ensures the pos-
sibility of continuous adjustments; thus, it is referred to as
a “closed loop”. By contrast, the ejection of the tentacles is
much faster (30–75 ms) and this precludes its control using
visual feedback; therefore, it is under an “open loop con-
trol”. This “seizure” by the ejection of the tentacles is the
only component of the attack that, once started, is inevita-
bly completed without any possibility of adjustments and/
or interruptions (for example when the position of the prey
changes; Messenger 1968; Duval et al. 1984).
Wells (1958), studying newly hatched cuttlefish, found a
decrease in the length of the delay before attacking a shrimp,
from about 2 min on the first occasion to 5–10 s on the fifth
Animal Cognition
and subsequent trials, in the absence of any change in the
movements. Latencies depended only upon the number of
attacks already made. Moreover, the sequence of the three
components is not necessarily completed, with the indi-
vidual showing a sudden loss of interest towards the prey.
In most cases, interruptions are caused either by a sudden
displacement of the prey (Messenger 1968) or by occasional
reflections visible on the glass sides of the tank (Wilson
1946). The first indication of individual differences in preda-
tory behaviour came from the study of Adamo et al. (2006),
describing consistent individual differences in the tendency
of cuttlefish to hunt with the first two arms raised. Finally,
in a meta-analysis on repeatability of behaviour (the fraction
of variation due to individual differences) across taxa, inver-
tebrates did not differ from vertebrates (Bell et al. 2009).
Given the foregoing, cuttlefish predatory behaviour is clearly
not fixed or invariant, but on the contrary, it shows an inter-
esting variability within the components of the attack (as
detailed by the above-mentioned studies). Here, we hypoth-
esise that this variation could be attributed to personality
differences.
Studying cephalopod variability in behaviour is also cru-
cial for their welfare, which requires detailed behavioural
assessments at the individual level (Tetley and O’Hara
2012). This is also prompted by the recent inclusion of
cephalopods in the European Directive 2010/63/EU on
the protection of animals used for scientific purposes, as
cephalopods have been given the same legal protection as
previously afforded only to vertebrates, with a consequent
need for further investigations and development of guide-
lines (Horvath et al. 2013; Smith et al. 2013; Fiorito et al.
2014, 2015).
This study first investigated between- and within-indi-
vidual consistencies of prey capture behaviour, including
success rate, accuracy of the attack, and the effect of experi-
ence. Then, the association of prey capture behaviour with
the personality dimensions identified in a previous analysis
(Carere et al. 2015) was tested.
Methods
Ethical note
Huntingford (1984), in her paper on ethical issues raised
by studies of predator–prey interactions when these involve
artificially staged encounters, recommended researchers “to
make sure that the behaviour is recorded accurately and
to explore the possibility of collaborative experiments”. It
is in this spirit that we conducted the present study, which
is entirely based on video clips recorded during a previ-
ous experiment (Carere et al. 2015), thus ensuring that a
maximum of information is gained and a minimum of suf-
fering caused.
Cuttlefish are visual carnivores, feeding on a wide vari-
ety of live prey. Although it is possible to train laboratory-
reared juvenile cuttlefish to eat dead prey (von Boletzky and
Hanlon 1983), wild-caught adult cuttlefish refuse to capture
and consume them (Darmaillacq et al. 2004). Furthermore,
the provision of live food promotes more “natural, positive
behaviours” (Tonkins et al. 2015; Yang and Chiao 2016).
These wild-caught adult animals (March, April 2011) were
kept in captivity for a limited amount of time (10 days for
acclimation plus 12 days for testing) and they were fed on
live fish, one per day, which in the majority of cases were
killed and eaten shortly after their introduction into the tank
(Carere et al. 2015). Furthermore, the number of subjects
was kept to a minimum and the experiments made as short
as possible to minimize the numbers of fish used (Hunting-
ford 1984).
While the original study by Carere and co-authors
preceded the implementation of the European Directive
2010/63/EU, it complied with the regulations of the Cana-
dian Council of Animal Care for animal research (University
of Lethbridge, Animal Welfare Approval n. 1106).
Subjects and housing
The present study involved 19 adult male cuttlefish
(mantle length 13 ± 0.4  cm, mean ± SEM), individually
housed in glass tanks covered on all sides by black plas-
tic (60 × 30 × 35 cm, capacity 60 l). The upper side was
equipped with a rectangular window that allowed the pas-
sage of artificial light to simulate the natural photoperiod.
Cuttlefish were maintained on a 12 h light–dark cycle (lights
on at 8.00 am), controlled by a timer connected to the arti-
ficial lighting system. They had been captured by nets off-
shore in the coastal area in the Central Tyrrhenian Sea (Italy)
during spring. Only males were selected, as females were
mature and their behaviour would have changed if egg laying
had occurred. Each individual was tested daily for 10 days,
at the same hour and in its own tank, in three different tests:
the “alerting” and the “threat” tests were performed in the
morning, whilst the “feeding” test, which is the focus of the
present study, was conducted at least 3 h later (Mather and
Anderson 1993). For details of housing and testing proce-
dures, see Carere et al. (2015).
In the “alerting” test, the black plastic lid of the tank was
opened and the observer (G.G.) brought his head over the
water surface, where the cuttlefish could see it clearly. He
looked directly at it for 1 min and then moved away. In the
“threat” test, the observer extended a long test-wooden stick
into the tank and briefly touched the cuttlefish with its end.
In both the “alerting” and “threat” tests, cuttlefish behaviour
was video-recorded for the subsequent 5 min.
13

At the beginning of the “feeding” test, a live fish (Mugil
cephalus, Linnaeus 1758; length 6–10 cm) was dropped
into the end of the tank opposite the one, where the cuttle-
fish was located. Cuttlefish behaviour was video-recorded
(Canon MV890) for the next 300 s to allow for subsequent
slow-motion analysis (0.7×, 420 s). Videos were scored by a
single operator (G.C.) with the software Observer 2.0 (Nol-
dus); scoring was stopped at prey capture. Ratings of this
operator were compared with those previously obtained (see
Carere et al. 2015) and the level of concordance was high
(ICC values ≥ 0.85). One or more attacks occurring within
5 min from prey presentation were counted as one hunting
sequence (i.e. from the start of the attention of the first attack
to the end of the seizure of the last attack).
Cuttlefish prey capture behaviour: the hunting
sequence and the attack
Cuttlefish predatory behaviour can be defined as a purpose-
ful series of movements in a manner that can lead to the cap-
ture of a prey. Cuttlefish predatory behaviour is divided in
two categories: the “hunting sequence” (Wilson 1946; Duval
et al. 1984) and the “attack” (Wilson 1946; Messenger 1968;
Duval et al. 1984; Boal et al. 2000; Adamo et al. 2006). The
term “hunting sequence” is defined as a single event involv-
ing a certain number of consecutive “attacks” to the same
target, usually by means of a single method of attack (either
arm grab or tentacle strike), until the cuttlefish catches the
prey or renounces. Our definition of “hunting sequence” is
equivalent to the term “capture” used by Wilson (1946) and
by Duval et al. (1984).
An “attack” is a single attempt to seize a prey during a
“hunting sequence”. Our definition of “attack” corresponds
to the same term “attack” used by Messenger (1968) and
by Boal et al. (2000); moreover, it corresponds to the term
“attempt” used by Wilson (1946) as well as by Duval et al.
(1984), and to the term “foraging event” used by Adamo
et al. (2006).
Each “attack” includes three components, termed “atten-
tion”, “positioning” and “seizure”, as shown in the Online
Resource 1 (see also the description provided in the “Intro-
duction”). Only in earlier works, the term “approach” was
used instead of the term “positioning” (Sanders and Young
1940; Boycott 1958). Notably, the terms “stages” (Sanders
and Young 1940; Wilson 1946; Boal et al. 2000; Adamo
et al. 2006) and “phases” (Wells 1958; Adamo et al. 2006)
have been used as alternative terms for “components” (Mes-
senger 1968).
Data collection
Scored behaviours were: components of the attack (dura-
tion of “attention”, “positioning”, “seizure”, as well as
13
Animal Cognition
latency to exhibit these patterns measured starting from
the time when the prey was introduced in the tank, plus
latency to “eat” it, i.e., when the fish touched the beak; e.g.
Sanders and Young 1940; Messenger 1968); position in the
tank (time spent at the bottom of the tank and down, in the
middle of, up in the water column—“ground”, “down”,
“middle”, “up” for brevity); postural elements (dura-
tion of “drooping arms”, “raised arms”, “splayed arms”;
Sanders and Young 1940; Boycott 1958; Messenger 1968;
Hanlon and Messenger 1988); locomotor elements (time
spent motionless and moving - “immobility”, “moving”
for brevity); body patterns (duration of “uniform light”,
“light mottle”, “weak zebra”, “dark mottle”, “deimatic”;
Holmes 1940; Boycott 1953; Hanlon and Messenger 1988,
1996). The latter serves a variety of purposes, from pri-
mary (cryptic displays) and secondary (threat displays)
defence to intraspecific communication (O’Brien et al.
2016; Brown et al. 2012).
The number of successful and missed tentacle shots (i.e.
errors) was also recorded (Messenger 1968; Duval et al.
1984).
Statistical analyses
PCA and Pearson’s correlations were performed using Sta-
tistica release 8 (StatSoft Inc., Tulsa, OK, USA). Since PCA
factors are built with mean zero and unitary standard devia-
tion (see Giuliani et al. 1994, 2004), their distribution is
unlikely to strongly deviate from normality, and therefore,
using Pearson’s correlation is acceptable. Bonferroni correc-
tions were not applied due to our small sample size (n = 19).
It has actually been shown that applying Bonferroni correc-
tions with small sample sizes will increase the probability
of making type II errors (failing to reject an incorrect null
hypothesis) to an unacceptably high level (see Nakagawa
2004). We calculated individual-based repeatability (RICC)
across trials during the feeding test by linear mixed-effects
models (LMM) using individual identity as a random factor
in SPSS 23.0 (see below). The remaining statistical analy-
ses were conducted using StatView 5.0 (Abacus Concepts,
USA). Data are expressed as mean ± standard error (SEM)
and statistical significance threshold was set at P = 0.05 (n.s.:
not significant).
The predatory performance of cuttlefish was described
quantitatively through the following parameters: predation
rate (N days in which one hunting sequence occurred/N total
days); success rate (N successful attacks/N total attacks);
accuracy of the attack (N of failed attempts before success-
ful attempt; Messenger 1968; Duval et al. 1984); and total
hunting time (i.e. actual time of predatory behaviour, calcu-
lated as the sum of the durations of attention, positioning,
and seizure).
Animal Cognition

Relationship between behavioural responses in a predatory
context
The relationship between behavioural responses exhibited
by cuttlefish in a predatory context (i.e. feeding test) was
investigated by running a PCA (named “PCA-Predation”)
on all tested individuals (n = 19). For each behaviour, an
individual mean value was calculated across days in which
one hunting sequence occurred (Table 1). The mean value
included the duration (D) of the measured behavioural vari-
ables and, in some cases, the latency to display them (L). For
a detailed explanation, see Carere et al. (2015). The follow-
ing 16 original variables were entered in the PCA: “atten-
tion” (L, D), “position” (L, D), “seizure” (L, D), “eat” (L),
“drooping arms” (D), “raised arms” (D), “uniform light”
(D), “light mottle” (D), “ground” (D), “down” (D), “mid”
(D), “immobility” (D), and “moving” (D). The body patterns
“dark mottle” (D) and “deimatic” (D) were almost never
recorded and were, therefore, excluded from the analyses.
The postural element “splayed arms” (D), the body pattern
“weak zebra” (D), and the position in the tank “up” (D)
had also to be excluded from the analyses, because too few
individuals displayed them.
PCA is a procedure that allows a reduction of the dimen-
sionality of a data set by replacing multiple inter-related
original variables with a few, new uncorrelated component
variables called “factors”. Each factor represents a linear
combination of the original variables, and it is constructed
to have a mean value of zero and a standard deviation of one.
The factors are extracted in order of decreasing percentage
of variation that they explain of the whole data set, so the
higher the variation explained by a given factor, the higher
the elongation of the data points along it. Note that, although
the scores of each factor are calculated by linearly combin-
ing all the original variables, factors differ with respect to
the regression coefficients (weights) assigned to the origi-
nal variables, which in turn are related to the correlation
coefficients between the factors themselves and the original
variables (see Table 2). The correlations between the PCA
factors and the original variables allowed us to assess: (1)
the differences between factors; (2) which original variables
are more influenced by variations in the underlying factor;
and (3) which original variables covary along the same
dimension. Therefore, this analysis allowed us to identify
the dimensions along which individual differences in cut-
tlefish predatory behaviour were maximal (PCA factors).
Finally, to investigate potential relationships between
predatory behaviour, performance and body size, corre-
lations were run between PCA factors and the following
parameters: predation rate, success rate, total hunting time,
and body size.
Correlation with personality dimensions in other
non‑predatory contexts
To allow for the assessment of the individual consist-
ency of behavioural patterns across different contexts (i.e.
“predatory context” and “non-predatory context”, based on
factor–factor correlation), we first had to run a new PCA
(named “PCA-Personality”) on raw data used in Carere et al.

Table 1  Measures of Behavioural variable Mean ± SEM CV RICC CI P

behavioural responses of
individual cuttlefish (n = 19) in Attention (L) 61.80 ± 15.00 105.77 0.36 (− 0.20, 0.75) 0.090
the feeding test
Attention (D) 11.15 ± 1.75 68.54 − 0.30 (− 1.9, 0.55) 0.680
Position (L) 75.06 ± 17.88 103.84 0.41 (− 0.12, 0.78) 0.057
Position (D) 3.59 ± 0.49 60.14 − 0.68 (− 3.4, 0.46) 0.814
Seizure (L) 77.38 ± 18.11 102.00 0.46 (− 0.05, 0.79) 0.036
Seizure (D) 0.72 ± 0.06 37.11 − 0.46 (− 1.99, 0.46) 0.779
Eat (L) 78.84 ± 13.73 75.91 0.37 (− 0.38, 0.79) 0.127
Drooping arms (D) 67.00 ± 19.51 126.91 0.26 (− 0.54, 0.73) 0.208
Raised arms (D) 32.12 ± 5.88 79.77 − 0.10 (− 1.27, 0.65) 0.472
Uniform light (D) 28.09 ± 10.19 158.18 0.31 (− 0.49, 0.76) 0.170
Light mottle (D) 56.16 ± 14.26 110.70 0.30 (− 0.47, 0.75) 0.176
Ground (D) 65.79 ± 19.21 127.24 0.65 (0.23, 0.88) 0.005
Down (D) 29.75 ± 9.04 132.51 0.098 (− 1.0, 0.69) 0.375
Mid (D) 4.71 ± 1.59 147.58 0.60 (0.14, 0.86) 0.010
Immobility (D) 73.22 ± 18.72 111.45 0.68 (0.31, 0.89) 0.002
Moving (D) 27.76 ± 5.05 79.35 − 0.43 (− 2.22, 0.50) 0.744

Values are mean latencies (L) and durations (D) ± standard error in seconds, the corresponding coefficient
of variation (CV) and individual-based repeatability (RICC) with 95% confidence intervals (CI) across five
trials. N = 13 for RICC (N = 12 for E at L). Significant values are highlighted in bold. See the “Methods” for
details on statistics and behavioural variables

13

(2015), using the variables measured in the “alerting” and
“threat” tests and discarding those related to the “feeding”
test; we also excluded from the new PCA two individuals
that, because of paucity of data, could not be included in the
“PCA-Predation” (the latter was run on 19 individuals whilst
the original PCA included 21 individuals). Pearson’s corre-
lations were then run to investigate the relationship between
behavioural patterns in the predatory context (i.e. the scores
from the PCA run on “feeding test” data; “PCA-Predation”)
and behavioural responsiveness in the non-predatory context
(i.e. the scores from the PCA run on “alerting” and “threat”
tests data; “PCA-Personality”).
Temporal profile
The analysis of the effect of experience on predatory behav-
iour was performed on the 16 original behavioural vari-
ables (the same that were used in the PCA, see above) using
repeated measures analysis of variance (ANOVA), with
“time” as the within subject factor. A logarithmic transfor-
mation was employed when dealing with latency data. For
the analysis of the temporal profile, a subset of individuals
(13 subjects) and a subset of days (5 days) had to be selected
in order to have a sufficient number of days in which one
hunting sequence occurred.
Inter‑individual variability
The analysis of inter-individual variability in predatory
behaviour was performed on all variables except those
for which an effect of experience was clearly present (see
previous paragraph). This analysis was performed on the
same subsets of individuals (13 subjects) and days (5 days)
selected for the analysis of the temporal profile (see pre-
vious paragraph). We calculated individual-based repeat-
ability (RICC) across trials in the cuttlefish responses dur-
ing the feeding test by intra-class correlation, calculated as
the proportion of phenotypic variation that can be attrib-
uted to between-subject variation (Lessells and Boag 1987,
Table 1). This was done by LMM.
Results
General descriptive analysis
On a total of 153 video clips that were analysed, a hunt-
ing sequence took place in 109, for a total of 176 attacks
(on average 9.3 ± 1.1 attacks per individual). 105 hunting
sequences out of a total of 109 resulted in prey capture,
while in the remaining 4, the cuttlefish gave up attacking
without capturing the prey. The predation rate and the suc-
cess rate were 71 ± 6% and 64 ± 4%, respectively.
13
Animal Cognition
As regards the accuracy of the attack, cuttlefish captured
the fish at first attempt in 59% of instances (of a total of 105
successful attacks), whereas they caught it at second attempt
in 26% of cases (Fig. 1a).
Relationship between behavioural responses
in a predatory context
In Table 1, we report the descriptive statistics as well as
the repeatability values concerning all the behavioural vari-
ables measured during the feeding test. These variables were
subsequently entered in the PCA. In Table 2, we report PCA
results and Pearson’s correlations between the first three fac-
tors of the PCA, run on all 19 individuals, and the 16 origi-
nal variables under investigation.
We selected the PCA factors that accounted for at least
70% of the total variance in the data, i.e. the first three fac-
tors (Giuliani 2017). The first factor of the PCA explained
about 53% of the total variance in the data, the second about
16%, and the third about 10%.
The first factor had a high negative correlation with
latency to attention, position, seizure and eat; moreover, it
had a high negative correlation with duration of drooping
arms, uniform light, light mottle, time spent on the ground
and immobility; it showed a moderate, negative correlation
with duration of “down” and “moving” (Table 2). In other
words, cuttlefish with high positive values on this axis dis-
played short latencies to attention, position, seizure, and eat;
moreover, they displayed short durations of drooping arms,
uniform light, light mottle, time spent on the ground, time
spent immobile, time spent down, and time spent moving.
Conversely, cuttlefish with high negative values on this axis
displayed long latencies to attention, position, seizure, and
eat; moreover, they displayed long durations of drooping
arms, uniform light, light mottle, time spent on the ground,
time spent immobile, time spent down, and time spent mov-
ing. Overall, the first PCA factor seems to differentiate indi-
viduals on the basis of their “speed in attempting to catch
the prey”.
The second PCA factor showed a high negative correla-
tion with duration of position and seizure, although it also
had a moderate, negative correlation with duration of time
spent down and in the mid of the tank (Table 2). Thus, ani-
mals with high positive values on the second axis displayed
short durations of behaviours such as position and seizure
and they spent a relatively short amount of time down and
in the mid of the tank. The opposite patterns held for cut-
tlefish with high negative values on this axis. Overall, this
axis seems to discriminate animals based on their “duration
of attack behaviour”.
The third axis showed a high negative correlation with
duration of attention and raised arms (Table 2). In other
words, animals with high positive values on this axis paid
Animal Cognition

a b
80 80

latency to attention (s)

60 60
frequency

40 40

20 20

0 0
0 1 2 3 4 1 2 3 4 5
number of errors days

c d
80 80
latency to positioning (s)

latency to seizure (s)

60 60

40 40

20 20

0 0
1 2 3 4 5 1 2 3 4 5
days days

Fig. 1  a Accuracy of the attack—number of failed attempts before components of the attack, i.e. attention (b), positioning (c), and sei-
successful attempt on a total of 105 successful attacks performed zure (d) over 5 consecutive days. Data are mean ± SEM. ANOVA:
by 19 individuals. b–d Temporal profile—latencies to display the 3 P < 0.01 (n = 13)

Table 2  Pearson’s correlations, Behavioural variable First axis (53.05% total Second axis (15.88% total Third axis
between the first three factors variance) variance) (9.59% total vari-
of the PCA, run on all 19 ance)
individuals, and the 16 original
variables under investigation Attention (L) − 0.938 0.480 0.242
Attention (D) − 0.315 − 0.132 − 0.752
Position (L) − 0.985 0.110 0.078
Position (D) − 0.077 − 0.786 − 0.063
Seizure (L) − 0.986 0.101 0.060
Seizure (D) − 0.148 − 0.819 − 0.005
Eat (L) − 0.895 0.003 0.241
Drooping arms (D) − 0.975 0.114 0.119
Raised arms (D) − 0.385 − 0.268 − 0.746
Uniform light (D) − 0.728 0.261 − 0.085
Light mottle (D) − 0.803 − 0.085 0.109
Ground (D) − 0.841 0.369 − 0.274
Down (D) − 0.601 − 0.599 0.345
Mid (D) 0.036 − 0.630 0.166
Immobility (D) − 0.960 0.130 − 0.059
Moving (D) − 0.687 − 0.376 − 0.154

Moderate to high correlations (> + 0.5 and < − 0.5) are highlighted in bold and were used to interpret the
meaning of the PCA factors
L latency D duration

13
 Animal Cognition

attention to the prey for short durations and had a low ten-
dency to raise and wave their arms, whereas the opposite
held for animals with high negative values on this axis.
Overall, the third axis seems to differentiate individuals on
the basis of the “duration of the attention towards the prey”.
Relationship between predatory behaviour,
performance, and body size
The predation rate and the success rate were positively and
significantly correlated with the first and the second factors
of the PCA, respectively, whilst the total hunting time was
negatively and significantly correlated with the third PCA
factor (Table 3). In other words, individuals who were faster
in attempting to catch the fish were also those that exhibited
predatory behaviour more often when the fish was presented.
Moreover, individuals who exhibited shorter durations of
attack behaviour, particularly “positioning” and “seizure”
(i.e. performing fewer attacks in a hunting sequence) had a
better performance in prey capture. Body size did not show
any significant correlation with any of the PCA factors, sug-
gesting that individual differences in predatory behaviour
did not reflect differences in body length. However, body
size showed a positive, significant correlation with the suc-
cess rate indicating that the attacks performed by bigger
individuals were more likely to result in the capture of the
prey.
Correlation with personality dimensions in other
non‑predatory contexts
The results of the new “PCA-Personality” (based on the
raw data used in Carere et al. 2015) were similar to those
found in the previous analysis (see Online Resource 2 and
3). The first three factors together explained about 77% of
the overall variation in the data: the first factor strongly cor-
related with measures of floating and activity; the second
factor was mainly correlated with measures of activity and
deimatic reactivity to a threat; and the third factor was still
strongly related to the frequency of changing colour during
the “alerting” and “threat” tests, although this time it was not
strongly correlated with the duration of escaping behaviour.
The first factor of the “PCA-Personality”, from the non-
predatory contexts, was positively and significantly corre-
lated with the second factor and negatively and significantly
correlated with the third factor of the “PCA-Predation”,
from the predatory context (Table 4). In other words, indi-
viduals who were more active in both the alerting and the
threat tests performed a lower number of attacks in a hunting
sequence (which is associated with higher success rate, see
above) and exhibited longer attention bouts.
Temporal profile
We observed a progressive reduction over time of laten-
cies to display attention (F4,48 = 6.915, P = 0.0002; Fig. 1b),
positioning (F4,48 = 7.260, P = 0.0001; Fig.  1c), seizure
(F4,48 = 6.975, P = 0.0002; Fig. 1d), and latency to eat the
prey (F4,44 = 2.716, P = 0.0417) over 5 consecutive days. The
delay before reacting when the fish was presented decreased
from about 60 s on the first occasion to about 10 s on the
third and subsequent ones. However, in subsequent trials,
cuttlefish did not improve their prey capture efficiency,
measured as total hunting time (F4,44 = 0.116, P = 0.9760
n.s.). No significant differences over time were detected for
the remaining behavioural variables (data not shown).
Table 4  Pearson’s correlations, between the PCA factors of the
predatory context (“PCA-Predation”, i.e. run across the feeding test
data; see Table 2) and the PCA factors of the non-predatory context
(“PCA-Personality”, i.e. run across the alerting and threat tests data;
see Online Resource 3 in the electronic supplementary material)
PCA-Predation PCA-Personality
First axis Second axis Third axis
First axis − 0.019 − 0.326 − 0.128
Second axis 0.557* − 0.307 − 0.014
Third axis − 0.522* 0.071 0.036
Moderate to high correlations (> + 0.5 and < − 0.5) are highlighted in
bold
* P < 0.05

Table 3  Pearson’s correlations, between the first three factors of the “PCA-Predation” and variables not included in the PCA (i.e. predation rate,
success rate, total hunting time, and body size)
Behavioural variable First axis Second axis Third axis Predation rate Success rate Body size

Predation rate 0.739** − 0.433 − 0.050 – – –

Success rate 0.408 0.506* 0.276 – – –
Total hunting time − 0.201 − 0.271 − 0.505* − 0.120 − 0.191 0.313
Body size 0.341 0.118 − 0.140 − 0.054 0.635** –

Moderate to high correlations (> + 0.5 and < − 0.5) are highlighted in bold and were used to interpret the meaning of the PCA factors
* P < 0.05; ** P < 0.01

13
Animal Cognition
Inter‑individual variability
Consistent individual differences over time in predatory
behaviour emerged as significant repeatabilities of latency
to seizure, time spent on ground and mid and time spent
in immobility. These repeatability values were all > 0.60
(Table 1).
Discussion
Variation in cuttlefish prey capture behaviour
This study confirms that, among cephalopods, cuttlefish are
not an exception to the pattern of animals showing consistent
individual differences in clusters of behaviour. The evidence
of consistent individuality in the predatory context adds to
other discoveries on the complexity of these animals (e.g.
tactical intraspecific deception, Brown et al. 2012; numerical
representation; Yang and Chiao 2016). In-depth analyses of
specific behaviour sequences, like the prey capture in cut-
tlefish, remind us that a variety of hidden influences may
control even those actions generally considered fairly fixed.
We highlighted a substantial variation in prey capture pat-
terns supposed to harbour little variability. Indeed, the first
three factors of the PCA explained about 79% of the total
variance in the data, which implies considerable individual
variation in cuttlefish’s behaviour during predation. The first
factor of the PCA showed that latency to attention, position,
seizure and eat covaried (with the same sign) with duration
of drooping arms, uniform light, light mottle, time spent on
the ground and immobility. This factor indicates that indi-
viduals displaying short latencies to attention, position, sei-
zure, and eat were usually those exhibiting short durations of
drooping arms, uniform light, light mottle, as well as those
spending less time immobile and on the ground. Moreover,
the second PCA factor showed that duration of position and
seizure covaried with time spent down and in the mid of
the tank. The third PCA factor showed that long durations
of attention covaried with prolonged time spent displaying
the postural element “raised arms”. Finally, although some
variables showed little or no repeatability, we found some
relatively high coefficients with more than half falling within
the most frequently recorded in both vertebrates and inverte-
brates (Bell et al. 2009). We acknowledge that this consistent
variation holds over a very short time interval (5 days), and
short-term repeatability is typically higher than long-term
repeatability (Bell et al. 2009). Therefore, it would be inter-
esting to test for longer time consistency.
The individual behaviour during predation related to
measures of predatory performance (i.e. predation rate,
success rate, and total hunting time), but was not affected
by body size. Specifically, individuals who were faster in
attempting to catch the fish were also those who exhib-
ited predatory behaviour more often when the fish was
presented. Moreover, individuals who exhibited shorter
durations of attack behaviour, particularly “positioning”
and “seizure” (i.e. performing a lower number of attacks
in a hunting sequence) had a better performance in prey
capturing. Although this strategy could be explained as a
trade-off (Chittka et al. 2009) between the success rate and
time, our analysis did not seem to support this hypothesis,
since the latency to display the three components of the
attack—first factor—and the duration of attention towards
the prey—third factor—were not correlated with the suc-
cess rate.
Finally, the attention component, during which cut-
tlefish tend to exhibit the postural display of “raised
arms”, was associated with the total duration of the hunt-
ing sequence. The postural element “raised arms” was
described by Hanlon and Messenger (1988) as follows:
“The first pair of arms is raised vertically upwards and
usually slightly parted. Often the second pair of arms is
raised at a slight angle so that from the side the first two
pairs of arms appear at right angles to each other. The
arms are sometimes dark. This posture has been described
in adults by Sanders and Young (1940), Boycott (1958)
and Messenger (1968)”. A similar result was reported
by Adamo et al. (2006) who found that (1) some cuttle-
fish almost always exhibited this postural element, while
others almost never adopted it, and (2) raised arms were
more likely to occur the longer the foraging event lasted,
regardless of the identity of the prey and prey context.
These differences emerged despite the fact that all cut-
tlefish had been reared in the same laboratory under the
same controlled conditions. The function of the postural
element “raised arms”, which is often observed during the
component of “attention” (Hanlon and Messenger 1988),
remains an area of active research (e.g. Hanlon and Mes-
senger 1996; Adamo et al. 2006). Hanlon and Messenger
(1996) suggest that it may serve some function during pre-
dation and Adamo et al. (2006) propose that individual
differences in its use may reflect differences in hunting
strategies between individual cuttlefish.
The absence of any significant correlations between body
size and PCA factors suggests that individual differences in
predatory behaviour may not depend on morphological dif-
ferences, although this should be taken with caution since
we recorded one single body measure. However, body size
showed a positive, significant correlation with the success
rate, indicating that the attacks performed by bigger indi-
viduals more likely resulted in the capture of the prey. Since
we do not know to which extent our sample represents size
variation in the cuttlefish population, further studies on a
bigger sample are deemed necessary to confirm the relation-
ship among these variables.
13

Success rate and accuracy of attack
To our knowledge, this is the first precise account of success
rate of prey captures and of accuracy of the attack on a fish
target by ejection of the prehensile tentacles. By contrast, the
previous studies evaluated the accuracy of the attack on both
shrimps and crabs by ejection of the tentacles (e.g. Messen-
ger 1968; Duval et al. 1984). The rate of successful attacks
at the first attempt recorded in the present study (59.0%) is
lower than that obtained by Messenger (1968) for shrimps
(81.0% and 91.0% in white and grey tanks respectively) and
by Duval et al. (1984) for shrimps (87.7% in glass tanks)
and crabs (84.6%). The lower accuracy found in the present
study was to some extent expected considering how fast fish
are. Besides, our results are also in accordance with some
qualitative observations by Duval et al. (1984) obtained on
a few mullet captures. As previously observed by Wilson
(1946) and Messenger (1968), failure to capture in the labo-
ratory setting was generally caused by the movement of the
prey at the moment of the tentacles ejection. If moving at
the moment that the tentacles are ejected, the prey will be
invariably missed (Wilson 1946). In accordance with the
previous observations, it is clear that the cuttlefish aims prior
to tentacle ejection and that the aiming programme cannot
be reset if the prey subsequently moves. Therefore, the con-
trol system is clearly an “open loop” one (Messenger 1968;
Duval et al. 1984).
On some occasions, the cuttlefish was probably distracted
by the reflected image of the prey on the glass, an observa-
tion also reported by Wilson (1946). Accordingly, in the
study of Messenger (1968), the group of cuttlefish kept in
white tanks, where reflections were more conspicuous, made
significantly more errors than the group in grey tanks (91.0%
and 81.0%, respectively), since the presence of reflected
light probably made the estimation of prey distance more
difficult. Indeed, cuttlefish are able to accurately estimate the
direction of the prey but not the distance; thus, some failures
to capture could be also caused by an underestimation of
the distance within the positioning component (Messenger
1968). Cuttlefish should be able to estimate distances as their
eyes diverge so that they have binocular vision. However, in
general they don’t have to judge the exact distance because
the tentacle ejection carries out past a pinpoint location—as
does the tongue of the chameleon—so exact accuracy is not
vital. Altogether, these results emphasise the complete reli-
ance on sight during hunting.
Decrease in latencies
Experience-dependent adjustments were detected only for
the latencies to display the three components of the attack.
Indeed, we observed a progressive reduction over the five
daily trials of latencies to react when the fish was presented,
13
Animal Cognition
from about 60 s on the first occasion to about 10 s on the
third and subsequent occasions, a clear evidence of learning.
Nevertheless, the decrease in the delay before reacting was
not concomitant with an improvement in cuttlefish prey cap-
ture efficiency (measured as total hunting time and latency
to eat the prey). A similar temporal profile was obtained
by Wells (1958) with newly hatched cuttlefish. Specifically,
when cuttlefish were fed daily on shrimps, no change in the
movements made in attacking was observed, but the delay
before reacting (i.e. the latency) when the shrimp was pre-
sented decreased from about 2 min on the first occasion to
5–10 s on the fifth and subsequent occasions. The length
of the delay before attacking depended upon the number of
attacks already made, regardless of the age of the animal,
whether it was hungry or not, or whether it had been allowed
to feed when it attacked. Thus, learning seems to play a role
in the predatory behaviour not only in juvenile individu-
als (e.g. Darmaillacq et al. 2014) but even in wild-caught
adult cuttlefish. Given the recent surge of interest (Sih and
Del Giudice 2012; Griffin et al. 2015; Guillette et al. 2017),
it would be worthwhile to explore the potential interplay
between personality and cognition in cephalopods.
Predation tactics are learned at a very early stage of the
life of cuttlefish (Dickel et al. 1997), especially when it
comes to potentially dangerous prey such as crabs. As the
immune system of cephalopods is not well developed, skin
wounds may lead to infections and even death; thus, a suc-
cessful predation technique is critical to cuttlefish survival.
The development of these tactics is based on trial and error
learning; on the contrary, no evidence was found that cut-
tlefish improved their predation techniques by observing
conspecifics (i.e. observational learning; Boal et al. 2000).
Correlation with personality dimensions in other
contexts
The first factor of the “PCA-Personality” (from the non-
predatory context) was positively and significantly cor-
related with the second factor, and it was negatively and
significantly correlated with the third factor of the “PCA-
Predation” (from the predatory context). This result sug-
gests that individuals who were more active in both the
alerting and the threat tests performed a lower number of
attacks in a hunting sequence and exhibited longer attention
bouts. These significant correlations highlight a consistency
between measures of cuttlefish personality in very different
contexts.
Behavioural syndromes can either extend across a broad
range of contexts (e.g. van Hierden et al. 2002; van Oers
et al. 2004) or be context specific (e.g. Coleman and Wilson
1998; for a review, see Sih et al. 2004). The present study
has revealed a broad syndrome, involving significant cor-
relations across different contexts (that is, exploration in a
Animal Cognition
non-social context was related to predatory behaviour and
performance in a feeding context).
Possible origin and consequences of individuality
in hunting behaviour
Our study investigated an aspect of individual variation that
could relate to individual feeding habits and prey choice.
Recent studies in different species (kestrels: Costantini et al.
2005; frogs: Araujo et al. 2009; octopuses: Mather et al.
2012) evidenced the presence, even within single popula-
tions, of individual differences in diet (prey species), likely
reflecting individual preferences or capabilities in capturing
some prey species instead of others. For example, parent
kestrels (Falco tinnunculus) can maintain consistent feeding
habits independent of prey type availability per se and it was
hypothesised that such prey choice variability may be part
of the individual personality (Costantini et al. 2005). The
marked individual differences in hunting behaviour found
in our study could relate to some pre-existing variation in
habitat and/or prey species choice, as demonstrated in the
octopus (Mather et al. 2012).
Each individual faces trade-offs based on factors like prey
encounter rate, resource value, prey escape rates, handling
times, and risk of predation on itself. However, as hypoth-
esised by Mather et al. (2012), individuals may calculate
these trade-offs in a different way. Cuttlefish have been
shown to have personality variation on three dimensions
(Carere et al. 2015) and this personality variation could well
affect individual trade-offs (and thus prey choice) in forag-
ing. This may occur, for example, through exploration or
directly through learning: personality variation such as risk
aversion could influence the exploration for prey and thus
the range of preys available to an individual; alternatively,
individual personality differences could affect the speed at
which individuals learn to avoid noxious prey (Crossland
2001).
Individual differences in behavioural patterns during pre-
dation may reflect differences in predation tactics among
different individuals. Such differences, which do not seem
to be equivalent in terms of fitness, since individuals scoring
higher on the second PCA factor were more successful in
capturing prey, could arise because of a combination of early
learning and genetic influences (Adamo et al. 2006) as also
hypothesised for other cephalopods (e.g. Sinn et al. 2001).
However, it may be possible that individuals who appeared
less successful in capturing fishes in this study could do
better when dealing with a different kind of prey. These dif-
ferences may be a starting basis for further studies aimed at
exploring how environmental influences may contribute to
produce individual differences in cephalopods.
Since male cuttlefish were caught in the wild and were
sexually mature, but age could not be distinguished, we
acknowledge that other factors may have contributed to the
observed differences in predatory behaviour. In particular,
individual’s previous experience with prey and potential
sensory-motor disorders associated with senescence may
constitute possible explanations for the observed variability
in predatory behaviour. Therefore, we must be cautious in
attributing the variation we observed solely to personality.
Finally, the presence of individualities could be useful for
refinement of cuttlefish welfare, because the individuals, and
not the species, emerge as the primary target of assessment
and adjustment (Mather and Carere 2018). The presence of
individualities in cuttlefish should be carefully considered,
not only in scientific research, but also in aquaculture and
public aquaria.
Acknowledgements  This research was partially supported by a Marie
Skłodowska-Curie Individual Fellowships (H2020-MSCA-IF-2014),
Project ID: 659106 (GROUPIND), to C. Carere. We wish to thank A.
Giuliani and F. Chiarotti for statistical advice, N. Francia and S. Falsini
for precious technical and administrative support. The work is part of
the BSc thesis of G. Cordeschi. Finally, we wish to thank the authors
of the original study (Carere et al. 2015).
Funding This study was funded by H2020-MSCA-IF-2014
(GROUPIND), Grant number 659106.
Compliance with ethical standards 
Conflict of interest  The authors declare that they have no conflict of
interest.
Ethical approval  All international, national, and/or institutional guide-
lines for the care and use of animals, applicable when the original study
by Carere et al. (2015) was performed, were followed. Specifically, the
original study complied with the regulations of the Canadian Council
of Animal Care for animal research (University of Lethbridge, Animal
Welfare Approval n. 1106).
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