Lateralization of aggression in fish

Behavioural Brain Research 141 (2003) 131–136
Research report
Lateralization of aggression in fish
Angelo Bisazza, Andrea de Santi∗
Department of General Psychology, University of Padova, Via Venezia 8, 35131 Padova, Italy
Received 1 March 2002; received in revised form 6 October 2002; accepted 7 October 2002
Abstract
Recent research has suggested that lateralization of aggressive behaviors could follow an homogeneous pattern among all vertebrates.
A left eye/right hemisphere dominance in eliciting aggressive responses has been demonstrated for all groups of tetrapods but teleost
fish for which data is lacking. Here we studied differential eye use during aggressive interactions in three species of teleosts: Gambusia
holbrooki, Xenotoca eiseni and Betta splendens. In the first experiment we checked for lateralization in the use of the eyes while the subject
was attacking its own mirror image. In order to confirm the results, other tests were performed on two species and eye preference was
scored during attacks or displays directed toward a live rival. All three species showed a marked preference for using the right eye when
attacking a mirror image or a live rival. Thus, the direction of asymmetry in fish appears the opposite to that shown by all the other groups
of vertebrates. Hypotheses on the origin of the difference are discussed.
© 2002 Elsevier Science B.V. All rights reserved.
Keywords: Lateralization; Aggression; Asymmetry; Fish
1. Introduction
Work done in the last three decades has demonstrated
functional specializations of the right and left side of the
brain in a variety of species belonging to all vertebrate
classes, suggesting that lateralization is a general feature
of the vertebrate nervous system [10,44]. One of the issues
raised by this accumulation of data concerns whether the
division of the labor between the two halves of the brain
have independently arisen multiple times during vertebrate
evolution or, alternatively, whether all extant vertebrates still
retain the functional left–right specialization which first appeared in some chordate ancestor [2,43].
Direct comparison of brain functionality among different
species is notoriously difficult, complicated by the fact that
the same function often relies on different neural substrates
in distantly related taxa. The use of a comparative behavioral
approach can reveal useful in these cases, allowing asymmetries for the same brain function to be compared among
a wide range of species by using simple behavioral tasks,
and permitting to observe left–right asymmetries in motor or
sensory information-processing without the need to practice
selective lesions or other invasive procedures.
∗
Corresponding author. Tel.: +39-49-8276915; fax: +39-49-8276600.
E-mail address: [email protected] (A. de Santi).
It should be noticed, however, that the comparison of
species at different taxonomic levels through behavioral tests
should be made with caution, as the same task may sometimes evoke a range of behavioral responses associated with
very disparate brain functions in species that are distantly
related or live in very different ecological conditions.
Data so far collected indicate that in some cases there are
striking similarities in the direction of lateralization among
vertebrates. For example, the production or perception of
species-specific vocalizations appear to be under selective
control of the left side of the brain in humans and monkeys
[9,32], mice [23], passerine birds [30], frogs [3] and catfish [24]. A selective involvement of the right side of the
encephalon in spatial analysis has been documented in several species of birds [13,33,41] as well as in humans [17]
and other mammals [16]. Moreover, the same side of the
brain appears to be preferentially involved in recognition of
conspecifics in a wide range of species ranging from fish to
humans [38,40,42].
However, not all studies support correspondence among
different species. Dominance in limb use appear extremely
variable even in closely related species and in similar tasks
[10,14,34]. In our species, mental rotation of objects is better
performed by the right hemisphere while the opposite was
found among baboons [15,45].
A few studies have specifically addressed the issue of
inter-specific comparison. Early findings generally support
0166-4328/02/$ – see front matter © 2002 Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 6 - 4 3 2 8 ( 0 2 ) 0 0 3 4 4 - 3
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A. Bisazza, A. de Santi / Behavioural Brain Research 141 (2003) 131–136
correspondence among species [7,40]. In a recent study
comparing 16 species of fishes at the same test, the direction of escape from a predator was the same in closely
related species but varied in distant taxa [8]. In another
study, opposite laterality in cooperative predator inspection was found in two closely related species, the eastern
mosquitofish, Gambusia holbrooki and the guppy, Poecilia
reticulata [18,19]. Both studies employed learned predators,
and it is possible that lateralization of memory storage is
more inter-specifically variable than other functions.
The first indication arising from these contrasting results
is that our understanding of the evolution of laterality is still
at the beginning; moreover, the difficulties in building up
a general theoretical model in order to make previsions to
be experimentally tested strongly suggests the need to get
more comparative data, extending research to more brain
functions and increasing the number of the studied species.
One of the functions that the most recent studies indicate as similarly lateralized in different vertebrates is the
control of aggressive behavior. Among Gelada baboons
(Theropithecus gelada) individuals direct more agonistic
responses to conspecifics on their left side [12], and this
may be the common condition of primates as suggested by
asymmetry in the expression of aggressive threat among
rhesus monkeys (Macaca mulatta) and by scar distribution in the baboon, Papio cynocephalus [22,27]. In young
chicken (Gallus gallus), stimuli presented to the left eye
are more likely to elicit copulation and attack responses
[36,37]. The left eye of the adult lizard Anolis also mediates
aggressive behaviors toward intruders more often than the
right eye [21]. Interestingly, in this study, changes of body
color associated with threat were found to be more marked
when the stimulus was seen with the left eye. During competition for food, toads (Bufo spp.) were found to deliver
more often tongue strike at eyes of conspecifics when these
appeared in the left lateral field of vision [34]. These evidences seem to imply a common left eye/right hemisphere
dominance in eliciting aggressive responses in all tetrapodes
and demand for an inquiry of the remaining largest group
of vertebrates, the teleost fishes. This study aimed at filling
this gap.
In the first experiment we studied eye preference while
attacking a mirror image in three species of teleost fishes.
To confirm the results of this experiment, additional tests
on two species were performed using a procedure similar
to that used to measure laterality of aggression in other
vertebrate taxa.
2. Materials and methods
2.1. Animals
Adult male fish belonging to three teleost species: Xenotoca eiseni, G. holbrooki and Betta splendens, were used in
the behavioral tests. All the three species commonly show
aggressive behavioral patterns and are widely used in lateralization experiments.
X. eiseni (Goodeidae) is a livebearing fish, living in
Central America’s small streams. Males are not territorial,
but often display aggressively during competition for females [4]. All the fish used in our experiments came from
a stock that was maintained in our laboratory. Fish were
kept in heterosexual groups made by 15–20 individuals
into 50 cm × 50 cm × 60 cm rearing tanks with artificial
lighting 16 h a day; water temperature was maintained at
25 ± 2 ◦ C and all fish were fed dry fish food and Artemia
salina nauplii twice a day.
The eastern mosquitofish, G. holbrooki (Poeciliidae) is
a livebearing fish, native of North America, introduced in
Europe at the beginning of this century. Male mosquitofish
do not defend a territory, but they are very aggressive towards other males, especially when competing for access to
females [5]. Mosquitofish were collected from a wild population (Idrovia, Camin, Padova, North Italy) and maintained
20 days in the laboratory before the experiments began.
Rearing conditions were the same as for X. eiseni.
Males of the Siamese fighting fish B. splendens (Belontiidae) are brightly colored, long finned fish, widely used as
a model species in research on aggressive behavior [39]. In
the wild, males of this species defend a territory with breeding purposes, showing very intense aggressive behaviors towards other males. Aggressive interactions usually start as
visual displays, but frequently end as fights which may cause
strong injuries or death. Fish used in the experiments were
obtained from a local pet shop; they were kept singly in
20 cm×30 cm×40 cm glass tanks and left to settle at least 20
days in the laboratory before the experiments began. Other
rearing conditions were the same as for X. eiseni.
Thirty four mature males (10 G. holbrooki, 12 X. eiseni
and 12 B. splendens) were used in the first test to measure eye
preference when attacking their own mirror image. Twenty
male mosquitofish and 10 male B. splendens were then tested
in order to measure eye preferences during free aggressive
interactions.
2.2. Behavioral tests
The apparatus used to measure eye preference during attack of own mirror image was made of a single glass tank of
68 cm × 68 cm × 37 cm (Fig. 1); to provide the subjects with
the image of a conspecific, a mirror (41 cm × 37 cm) was
placed vertically and spaced 1 cm out of one side of the tank,
while all the remaining sides were externally covered using
green, plastic panels. In order to hide the mirror while acclimatizing the subjects to the experimental tank, an opaque,
green plastic partition could be raised or lowered into the
space between the mirror and the tank glass. An observation
window (10 cm × 37 cm) could be opened in the central part
of the covering panel at the side opposite to the mirror, allowing us to record behavior without disturbing the subjects (the
observer was placed in the dark). Above the test apparatus
A. Bisazza, A. de Santi / Behavioural Brain Research 141 (2003) 131–136
Fig. 1. Drawing of the apparatus used to check for asymmetries in eye
use during aggressive behaviors toward a mirror image (M: mirror; OP:
opaque plates; WA: window area).
a video camera was mounted to videotape fish’s behavior.
A hourglass-shaped, glass-made swimway (see Fig. 1) was
created in order to divide the experimental tank into two
distinct areas: one to the window side, the other to the mirror side. Males were singly introduced into the swimway
and left to acclimatize for 24 h before the test began (the
mirror was covered during this period). In order to enhance
X. eiseni and G. holbrooki aggressive responses, two groups
of two females were introduced into the adjacent zones outside the swimway on the window side. Two green plastic
panels were angled so as to cover the sight of females while
the test fish were in the mirror area; subjects could thus see
the females only when swimming on the window side of
the tank. As males of B. splendens always display intense
aggressive behaviors toward their mirror image, females
were not necessary and so the lateral zones were left empty.
To perform the test, it was waited for the subject to swim
into the cleft area then the partition hiding the mirror was
raised. As the image of the “rival” appeared on the mirror,
the subject entered the mirror area and tried to attack its own
image; at the end of a single attack sequence, the covering
partition was lowered and it was waited for the fish to swim
back to the cleft area. The eye used to fixate the mirror image while attacking it was then scored using frame by frame
analysis of videotapes. Aggressive interactions were distinguished from simple shoaling by the presence of specific
behaviors and aggressive displays, so as a brighter color,
fins’ extension, and spreading of the opercula. A frequency
of use of the right monocular visual field was estimated.
An index of eye use was calculated as: (number of right eye
use)/(number of left eye use + number of right eye use). The
cases in which the fish remained perpendicular to the mirror
were not used in the analyses. Inter-rater reliability for this
behavioral test had been already calculated by Bisazza et al.
[6]; the correlation was found to be very high (r > 0.99).
133
A normal test session was composed by 30 trials on each
fish, but this revealed to be possible only for B. splendens and
G. holbrooki as all interactions with the mirror image were
of aggressive type. Males of X. eiseni did not always perform
aggressive behaviors while viewing their mirror image, and
they were therefore tested using a 50 trials schedule (a mean
of 34.83 (S.D. = 8.23) valid aggressive interactions was
obtained on each fish). In order to check for possible turning
biases not related to aggressive responses, eight additional
male Xenotoca were tested with the same apparatus and
procedure but without the presence of any mirror.
The experimental set up used to test eye preference during free aggressive interactions in G. holbrooki was made by
a glass tank of 68 cm × 68 cm × 37 cm placed in a darkened
room; water level inside the tank was set at 30 cm in depth
and the tank’s bottom was covered with 2 cm of fine gravel.
Two fluorescent lamps (18 W) provided illumination. Two
identical tanks were used. Above each tank a video camera was mounted to videotape fish’s behavior. Mosquitofish
were randomly divided in two groups of 10 fish; each group
was introduced into one of the experimental aquaria and left
to settle for 24 h. In groups of this size hierarchies are generally not established and all fish attack the others with similar frequency.1 However, prior to score the data we checked
by using slow motion that in each group there had been at
least five males simultaneously performing attacks. At the
end of the settling period, behavior of fish was recorded
twice a day on both tanks for a 10 min period; recordings
were repeated during 2 consecutive days, obtaining a sum of
80 min videotapes. Eye preference during aggressive events
was then scored on the videotapes according to the following categories:
(a) the visual hemifield occupied by the target fish just before an attack;
(b) the eye used to watch the rival during typical aggressive
displays, in which the two fish rotated while being in a
tail-to-head carousel position.
In order to check for eye preference during free aggressive interactions in B. splendens, a green, octagonal, plastic
arena of 27 cm × 24 cm × 32 cm was used as experimental apparatus. Males were confronted in pairs using a round
robin procedure forming pairs only with males of similar
sizes. Light was provided by four fluorescent lamps (18 W)
placed on the top of the arena. The testing arena could be
divided into two identical parts by an opaque partition that
allowed us to isolate subject fish from each other during acclimation to the new environment. The two males were introduced into the apparatus (one on each side of the partition)
and left to acclimate for 30 min before the test began. The
partition was then raised and fish were left free to interact.
Test sessions lasted for 20 min, but tests were stopped, and
fish divided, if aggressive interactions became so violent to
1
Bisazza, unpublished data.
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A. Bisazza, A. de Santi / Behavioural Brain Research 141 (2003) 131–136
risk injuries for the subjects. Behavior of fish was recorded
by a video camera which was mounted above the apparatus,
and laterality of aggression was then scored using the same
categories as before.
3. Results
3.1. Eye preference during attack of own mirror image
Analysis of grouped data revealed no significant statistical
difference among the three species (ANOVA: F (2, 31) =
0.121, NS). Species were pooled and there was clearly a
preferential use of the right eye during aggressive interactions (one sample t-test: t (33) = 3.9, P < 0.001). Separate analysis of single species confirmed the previous results
(one sample, one tailed t-test: B. splendens, t (11) = 2.0,
P = 0.034; X. eiseni, t (11) = 2.1, P = 0.032; G. holbrooki, t (9) = 2.8, P = 0.011) (Fig. 2). Analysis restricted
to the first 10 responses gave the same results (one sample t-test: t (33) = 3.7, P < 0.001), suggesting that there
are no time depending changes in the lateralization pattern.
Male X. eiseni tested without any mirror presence showed
no laterality biases (one sample t-test: t (7) = −1.2, NS).
The comparison between X. eiseni tested with or without
the mirror revealed that the laterality bias was indeed due to
the presence of a mirror image (t-test for unequal variances:
t (13.9) = 2.34, P = 0.035).
3.2. Eye preference during free aggressive interactions in
G. holbrooki
A sum of 92 attacks and 29 tail-to-head displays were
observed on one tank, 69 attacks and 26 tail-to-head displays
on the other one. Preference in eye use during aggressive
Fig. 3. Eye use during attacks or aggressive displays to a rival male in
G. holbrooki and B. splendens.
interactions was similar in the two experimental tanks; as
there were no statistically significant differences of laterality
in the attacks (χ 2 (1) = 0.019, NS), or displays (χ 2 (1) =
2.15, NS), data coming from both tanks were thus pooled
together. Mosquitofish showed a significant preference to
attack a rival when it was on the right hemifield (total number
of attacks: N = 161; right eye attacks: N = 97 (60.2%);
χ 2 (1) = 6.76, P = 0.009); no significant eye preference
were found for aggressive displays (total number of displays:
N = 55; right eye displays: N = 29 (52.7%); χ 2 (1) = 0.16,
NS) (Fig. 3).
Fig. 2. Eye use while attacking a mirror image in the three species.
A. Bisazza, A. de Santi / Behavioural Brain Research 141 (2003) 131–136
3.3. Eye preference during free aggressive interactions in
B. splendens
A sum of 14 encounters was performed; there were on
average 16.86 (S.D. = 10.90) attacks and 5.28 (S.D. =
4.03) displays per test. Fish showed a highly significant right
eye preference when attacking the rival (right eye attacks:
65.07% (S.D. = 9.2%); t (13) = 6.131; P = 0.001). The
analysis revealed a preference for the right eye when performing tail-to-head displays, but the difference is not fully
significant (right eye displays: 64.78% (S.D. = 29.68%)
t (13) = 1.863; P = 0.085).
4. Discussion
The results of the first experiment demonstrate that laterality in the use of the eyes strongly affects aggressive interactions in teleosts: our fish showed a marked preference for
attacking a rival when it entered the right hemifield, and this
right eye preference was the same for all the three species
we tested. The direction of asymmetry in fish appears the
opposite to that shown by all the other groups of vertebrates,
in which a preference for the left eye (i.e. specialization of
the right side of the brain) seems to be the most common
condition (see Section 1). The results could not be attributed
to a different procedure employed (mirror image as stimulus) since results were confirmed using a method similar to
that used for the study of laterality of aggression in the other
species [21,34].
It could be reasonably argued that at a certain point of
evolution in the passage from fish to amphibians there might
have been a shift in control of behavior related to agonistic
responses. Nonetheless, even if some indications claimed for
a common involvement of amygdala and hypothalamus in
neural control of aggressive responses among all vertebrates
[11], different types of intra-specific aggression behavior
might have distinct underlying neural mechanisms and might
be differently modulated by previous experience or by other
emotions [25–31].
It should also be noted that aggressive behaviors do not
refer to the activation of a single, simple, neural circuitry,
but result as an integrated output merging several cognitive
and motor functions. Thus, our results do not necessarily
suggest an asymmetry in neural control of aggressive behaviors, but rather a lateralization of some cognitive functions
which have to be activated in order to perform a complete
aggressive response.
Our results appear to be different from what reported by a
previous study [20], in which no population-level lateralization have been found for aggressive responses in B. splendens. It has to be noticed, however, that in the experiment
of Cantalupo et al. [20] the mirror used to simulate the rival had been placed horizontally on the floor of the tank,
thus forcing the subject to lie on one side and maintain an
unnatural position in order to attack its own mirror image.
135
It is possible that the different results may depend on the
different experimental conditions used in the two studies.
It has been argued [28,35] that alignment in the direction of asymmetries in different species would be the consequence of a general specialization of the left eye/right
hemisphere for immediate responses and behaviors having
emotional content, paired with a specialization of the right
eye/left hemisphere for responses that require the animal to
consider the consequences of its action and to inhibit some
responses while making decisions. Rogers [35] classified
the aggressive responses as belonging to the first category,
but this could not be true in all cases. In many species, the
crucial information needed to decide whether to attack or
not a rival (i.e. the prior residence on territory, the resource
value or the outcome of previous encounters) are available
to the subject long time before actually engaging the fight,
and emotional responses may thus prevail at the time of attack. Fishes, however, usually live in large aggregates with
individual recognition being a rare occurrence [26]; in addition, because of indeterminate growth, fishes show large
individual variation in size and body size is the main predictor of fight outcome in most species. It could be therefore
possible that a continuous inhibition of attack (which should
be mainly of concern for structures on the left side of the
brain [1,28]) is maintained till the very last moment, until a
correct, visually- or lateral line-made, short-distance assessment of the opponent’s body size is done. To answer these
questions it seems necessary a more direct investigation of
the asymmetries in the neural structures associate with control of aggressive behavior as well as an extension of behavioral studies to include other taxonomic groups within both
fishes and amphibians.
Acknowledgements
We thank R. De Carlo and M. Dadda for their help during the experiments, M. Dadda, F. Neat, G. Vallortigara and
two anonymous referees for reading and commenting on the
manuscript. The research was supported by a grant from Italian Ministry of University and Scientific Research (MIUR)
to A.B.
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