ISSN 0032-9452, Journal of Ichthyology, 2006, Vol. 46, Suppl. 2, pp. S235–S242. © Pleiades Publishing, Inc., 2006.
INTRODUCTION
Functional laterality (bilateral asymmetry) of the
vertebrate nervous system relates to the development of
their adaptive behavior and cognitive functions (Bianki,
1985; Bianki and Filippova, 1987). That is why the
study of evolution and primary displays of functional
laterality become an important problem of evolutionary
biology (Vallortigara et al., 1999) at the early stages of
the lower vertebrates' evolution, particularly in fish.
Numerous investigations of behavioral responses’ laterality
in teleosts were carried out to date (Bisazza
et al., 1998b). The aim of these investigations is to clarify
the origin and paths of the evolution of behavioral
laterality, its dependence on the asymmetry of brain
functions and morphological traits, its adaptive value
and the inter-relations of laterality of different behavioral
responses. At the same time, despite the presence
of extensive experimental data, the attainment of this
aim is obstructed by variability of behavioral laterality
caused by their dependence on many factors influencing
fish behavior. Our review is an attempt to systematize
the present data on fish behavioral responses in
which laterality is manifested, its dependence on the
sing of these responses, on the motivational state of the
fishes themselves and on external factors. At the same
time, we do not attempt to give the full bibliography on
this research area but concentrated our attention on
those publications that, in our opinion, most completely
demonstrated the variability of laterality and the problems
related to its experimental studies.
1. Group and Individual Laterality
Usually for qualitative assessment of behavioral laterality
a so-called coefficient of laterality is used: CL =
[R
−
L]/[R + L], where R and L denote the parameters of
reactions associated with the choice of either right or left
direction, respectively. For example, while studying the
laterality of fish motion in a round aquarium, the R symbol
denotes the distance with which fish went for a certain
time clockwise (“to the right”) and L symbol—the distance
counterclockwise (“to the left”) (Nepomnyashchikh
and Gremyatchikh, 1993). To compute CL values, the
time spent by fish moving clockwise or in the opposite
direction may be used instead of distance (Bisazza et al.,
1997b). While studying the responses to different objects,
R and L denote, respectively, the number of right and left
turns of fish relative to an object (Bisazza et al., 2000).
If the mean CL value in a group of specimens differs
statistically significantly from zero, then it is common to
say that the laterality is of group type (Bianki, 1985). If
in the repeating experiments the same individual prefers
some definite direction, it is commonly treated as an
indication of an individual laterality in animals (Bianki,
1985; Bianki and Filippova, 1987). As we will see later,
both types of laterality may be present in the same sample
of fish where individual laterality of some specimens
does not necessarily coincide with group laterality.
2. Laterality of Fish Responses
to Various Objects
Group laterality.
Probably, group laterality is most
evidently manifested in the fish when they respond to
objects that they see in the aquarium. Response to their
Variability of the Behavioral Laterality in Teleostei
(Pisces)
V. A. Nepomnyashchikh and E. I. Izvekov
Papanin Institute of Biology of Inland Waters, Russian Academy of Sciences,
Borok, Nekouzskii raion, Yaroslavskaya oblast, 152742 Russia
e-mail: nepom@ibiw.yaroslavl.ru
Received January 10, 2006
Abstract
—Factors causing variability of behavioral laterality in Teleostei are reviewed. The laterality has been
revealed in many fish species belonging to various families. The best ever demonstrated example of the laterality
is the different use of the right and left eyes when a fish responds to different visual objects. Magnitude and
sign of the laterality differ in fishes of different species, gender, and age. Also, an observed laterality depends
on how familiar a stimulus is to fishes and what it means to them, as well as their motivational level and various
behavioral traits. Therefore, comparisons of the laterality among different fish species should be based on
experimental methods that also take into account those behavioral differences among them that are not directly
linked to the laterality.
DOI:
10.1134/S0032945206110142
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own reflection in the mirror was studied in eight species
belonging to five teleost orders. Fish preferred to move
along the mirror in a way that allowed them to observe
the reflection with their left eye (Sovrano et al., 1999,
2001). However, in general, such group laterality may
have a different sign in different species (see below).
Moreover, different populations of the same species
may differ in this respect. For example, during experiments
Brachyraphis episcope
(Poeciliidae) and
Rivulus
brunneus
(Cyprinodontidae) caught in water bodies
with high abundance of predators used the right eye to
track the predator. At the same time the specimens from
water bodies with low predator pressure exhibited no
preference of either eye. This shows that manifestation
of behavioral laterality may depend on ecological factors
in fishes' natural habitats (Brown et al., 2004). It
should be noted, however, that it is uncertain if the
observed differences in laterality were caused by inherited
factors or a fish’s individual experience.
Quite often fish of the same species, for example,
those from family Poeciliidae use their right and left
eye for different purposes. Thus, females of
Gambusia
holbrooki
track their reflection in the mirror and the
free space predominantly with their left eye. However,
while being close to the predator, they usually turn to it
with their right eye (De Santi et al., 2001). Furthermore,
different functions of the right and left eye complement
one another: females get closer to the predator (observing
it with their right eye) if they see their own mirror
reflection from the left. Obviously, the mirror reflection
is interpreted as an indication of the presence of a conspecific
specimen (Bisazza et al., 1999). On the other
hand,
G. holbrooki
, as well as
Xenotoca eiseni
, may
display aggression towards their own mirror reflection
or another fish. During aggressive displays in most
cases, they turn to an opponent with the right eye
(Bisazza and De Santi, 2003).
Laterality in the use of either left or right eye
depends also on the object novelty. As the fish of different
species get accustomed to the object, they may
more often turn to observe it with another eye (CL sign
changes). In other cases habituation leads a fish to
observe the object using its right and left eye with equal
frequencies or to turn to the object directly watching it
with both eyes simultaneously (in both cases CL is
close to zero). At the same time laterality of fish
response to its own reflection vanishes after staying in
an aquarium with a mirror for five minutes, probably as
a result of habituation (Sovrano et al., 2001). It was
shown also that
Brachydanio rerio
(Cyprinidae) turns
to an unfamiliar object in such a way that it is being
observed by the frontal sector of the right eye’s field of
view. On the contrary, after the same object was presented
to the fish for the second time, the frontal sector
of the left eye’s field of view is being used predominantly
(Miklòsi et al., 1997). When adult
B. rerio
are
given small color balls for the first time, the fish observe
them mainly with the right eye and then try to bite them.
After the ball is given repeatedly, right eye preference,
as well as bites, disappears and fish orientate themselves
relative to the object in such a way that they
observe it with both eyes simultaneously. However, if
the fish are given a ball of a different color, the preference
of the right eye is restored and bites restart
(Miklòsi et al., 1997; Miklòsi and Andrew, 1999;
Miklòsi et al., 2001). Therefore, fish predominantly use
the right eye when they encounter an unfamiliar object.
Further, for observation of a familiar object, they also
use the left eye. Such forms of behavioral laterality can
be seen even in early fry of
B. rerio
(Watkins et al.,
2004; Barth et al., 2005).
Responses related to other organs of sense and not
only vision may also be lateral (Andrew and Watkins,
2002). Thus, blind cave fish
Astyanax fasciatus
show a
clear tendency to turn to an unknown object (protrusion
on the side of the aquarium) that is sensed by the lateral
line with their right side. This evidences the preference
of right body side lateral line organs for the studying of
new objects. However, after fish get accustomed to the
experimental setup and are habituated to the object, this
preference vanishes (Burt de Perera and Braithwaite,
2005).
Individual laterality.
As a rule, the presence of
group laterality in a given species of fish does not mean
that all specimens behave themselves in a similar manner.
In the aforementioned example with
G. holbrooki
(De Santi et al., 2001), the group laterality was determined
by the CL sign of individual laterality in the
majority of specimens while the lesser part of specimens
behaved in an opposite way or did not display laterality
at all. In some other cases, only individual laterality
may be observed, e.g., in Siamese fighting fish
(
Betta splendens
, fam. Anabantidae). In repetitive trials
males turned with the same eye, both to their own mirror
reflection during aggressive displays and to females
during courtship. The numbers of males preferring
either right or left eye was approximately equal (Cantalupo
et al., 1996). However, further experiments with
another sample of specimens showed that group laterality
may take place also in the aggressive behavior of
fighting fish: the majority of males turned to their own
reflection or to their opponent with the right eye
(Bisazza and De Santi, 2003). Such differences in the
results of different experiments with specimens of the
same species show that behavioral laterality is a variable
characteristic of behavior, which probably
depends on many factors including those not considered
by researchers (see Section 4).
Conclusions.
Lateral response to objects in the
environment is a result of preferential use of one body
side sensory organs (the eyes first of all) for evaluation
of unfamiliar and potentially important objects. The
presence of laterality and its sign depend on the fish
species and its gender, object novelty, and also on the
form of behavior to which the object is related (foraging,
predator avoidance, courtship or aggression).
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3. Laterality of Obstacle Detouring
Group laterality.
When fish meet an obstacle, they
make a detour of it either from right or left and, in the
choice of detouring direction, the group laterality is
manifested. This laterality was studied in 16 fish species
belonging to 13 families (Bisazza et al., 2000). The
obstacle represented a barrier made of vertical bars.
The fish were able to see through the barrier a model of
a predator against which the defense response was
developed beforehand. After the learning period, the
fish avoided the barrier in order to inspect the predator.
Each fish was placed in front of the barrier ten times
and the direction preference was determined as the difference
between numbers of right and left turns. The
representatives of 10 out of 16 species exhibited consistent
group tendency to turn to a definite direction. It was
also revealed that, in species of the same family, the
signs of group laterality coincide more often than in the
species belonging to different families.
It was also shown that the direction of obstacle
detouring depends on the nature of the objects that fish
see through the barrier. For instance, males of
G. holbrooki
exhibited a constant tendency to left turns if
either females or a predator model were beyond the barrier
but no preference was observed if other males or
open space were there. The trend to a left turn had also
vanished in the case if the barrier was U-shaped and
males, when avoiding it, were compelled to swim in the
opposite direction from the target. Finally, if the barrier
was not transparent, males preferred to turn right.
These results assume that the laterality of turns when
fish make a detour of an obstacle reflects the asymmetry
in eye functions. The objects that cause an interest are
tracked by the right eye (resulting in left turns in front
of the barrier), while, in the case of a nontransparent
barrier, the same eye is used for tracking the open space
not protected by the barrier (Bisazza et al., 1997c).
The data obtained as a result of similar trials with
poecilid fishes (
Gambusia nicaraguensis
,
Poecilia
reticulata
,
Brachyraphis roseni
(Bisazza et al.,
1997c), and
Girardinus falcatus
confirm that the laterality
of obstacle detouring is related to different eye
functions (Bisazza et al., 1998a). At the same time preferable
direction of the obstacle detouring differs in different
species even if the object beyond the barrier has
similar importance (e.g., females). In other words, the
sign of laterality is species-dependent.
Preferable direction of obstacle detouring may
change and even any preference may vanish along with
habituation of fish to experimental conditions, including
the objects placed beyond the barrier (Bisazza et al.,
1997c). Besides, the direction of detouring depends on
the level of fish motivation. For example, females of
G.
holbrooki
and
G. falcatus
that saw males beyond the
barrier did not exhibit a preference towards any direction
if they were kept together with males before the
experiment. However, after a two month-long keeping
apart from males, they had shown a tendency to turn left
which can be explained by a higher level of sexual
motivation in females (Bisazza et al., 1998a).
Choice of motion direction in the T-maze may also
be lateral in fish which is, perhaps, caused by the same
factors as in the case of the obstacle detouring. During
repeated trials in the maze, some young specimens of
Nile tilapia (
Oreochromis niloticus
; Cichlidae) show
consistent preference to right turns, while others do not
exhibit any preference (Gon alves and Hoshino,
1990a, 1990b).
Individual laterality.
If in case of obstacle detouring
the fish of any species exhibit the group laterality, it
does not mean that all specimens prefer the same direction
of detouring. The results of the experiments given
above (Bisazza et al., 2000) have shown that, in any of
the species studied, there are specimens showing stabile
preference to either right or left turns. In other
words, in all these species, the individual laterality of
obstacle detouring is presented. The group laterality
appears due to an uneven ratio of “right” vs. “left” specimens.
The group laterality is more pronounced in
social fish species which, according to Bisazza et al.
(2000), is due to the necessity to coordinate motions of
individual fish in school, while in the solitary living
species, only individual laterality presents.
Conclusions.
Most likely, the choice of a turn direction
during the detour is not an independent manifestation
of behavioral laterality. It relates to the asymmetry
of right and left eye functions during the study in the
environment of the objects differing in their novelties
and importance. Even if there are no specific objects
within the fish visual field (as in case of the detouring
of a nontransparent barrier), a determined eye is used to
check the unknown and potentially dangerous space.
4. Rotational Laterality
Group laterality.
One of the most common methods
to reveal behavioral laterality consists of the registration
of motion direction of an animal along the
perimeter of the circle enclosure or in a ring corridor
(rotational laterality). Numerous reports on group rotational
laterality in fish exist. Lapkin and coworkers
(1989) placed in a round aquarium a number of juvenile
roach (
Rutilus rutilus
) and bream (
Abramis brama
)
caught in the wild. Most often, this fish moved counterclockwise.
This phenomenon lasted about 25 days.
Before the known direction of motion was finally established,
changes of clockwise and counterclockwise
coordinated fish motions were observed. This coincided
in time with the period of increased locomotory
activity during the spring and fall migrations of juveniles
of these species and was absent in other times of
the year. Authors assumed that within the limited
aquarium space and at high fish density the need to
increase locomotory activity is realized in a form of a
coordinated one-way motion.
c˛
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It was similarly shown that marine fish of different
species, placed in large amounts in the circle enclosure,
swim along its perimeter in most cases clockwise, less
often counterclockwise or change direction by an irregular
manner (Suyehiro and Takizawa, 1968). It was also
noted that encaged bleak (
Alburnus alburnus
; Cyprinidae)
(Kuznetsov, 1975), smelt (
Osmerus eperlanus
;
Osmeridae) under natural conditions (Permitin and
Polovkov, 1975), and anchovy (
Engraulis encrasicholus
; Engraulididae) in open sea (Borisov, 1955) tend to
concentrate around the submerged source of light,
moving around it clockwise.
In all these experiments, the interrelations of fish
may have influence on both extent of manifestation of
rotational laterality and the fact of its appearance. However,
similar group laterality can be seen in solitary
specimens as well. The majority of juvenile specimens
of Mozambique tilapia (
Oreochromis mossambicus
;
Cichlidae), placed one at a time in a round aquarium,
exhibited preference to a clockwise motion (Hepomnyaschikh
and Gremyatchikh, 1993). Similar preference
was revealed in mosquitofish (
G. holbrooki
) (Bisazza
and Vallortigara, 1996, 1997).
In the cited works, as well as in the majority of other
similar studies, functional laterality in fish was determined
based on the result of a single experiment, and
the duration of the majority of such experiments did not
exceed 15 min. In fact, in all these experiments, a part
of the specimens moved in the direction opposite to the
direction of motion of the majority of fish. However,
this does not mean that differences in preferable direction
are caused by individual variability (e.g., genetic,
age, or gender) of specimens in the studied sample. As
it will be shown below, preferable direction may change
in the same specimen during the experiment. Such like
variability could affect CL, especially if the duration of
experiment is short.
Dependence of group rotational laterality on
sources of light.
The majority of researchers studied
rotational laterality in fish either under natural lighting
conditions or using the point source of light placed
above the center of the aquarium or cage. One may
assume that in these cases rotational laterality represents
the response to a light source: fish may interpret it
as either the sun (the angle to which serves as a reference
point during migrations) or as an unknown object
that causes interest. These assumptions were tested by
several researchers. Migrating fish
Cheirodon pulcher
prefer to move in a ring corridor clockwise in the presence
of a light source above the center of the enclosure.
If this source was substituted then by diffuse light, the
above mentioned preference remained unchanged.
However, if the fish was placed in the diffuse lit corridor
just from the very beginning of the trial, they do not
exhibit any directional preference (Levin and Gonzalez,
1994).
Similarly the hypothesis concerning the sun-compass
navigation in females of
G. holbrooki
(Bisazza and
Vallortigara, 1996) was tested. The experiments were
carried out in a circle aquarium with a light source
above its center. It was presumed that fish interpret the
light source as the sun at the angle to which they may
have to orient under natural conditions, moving off the
shores when avoiding predators. To test this assumption,
the females from the natural population were
observed during different day times differing in the sun
positions. Consequently, the direction of fish motion in
relation to its position must be also be different. During
the daytime, females preferred to move counterclockwise.
In the morning, they moved clockwise which
always corresponded with their movement off the
shores (with respect to the sun position in their natural
habitat). The preference in the direction was revealed in
males neither in the morning nor in daytime. However,
authors explain this by the fact that mosquitofish males
are subject to predator attacks less often (Bisazza and
Vallortigara, 1996). If the light source above the aquarium
center was substituted by three sources placed on
its periphery, then rotational laterality in the same
females disappeared. Finally, laboratory-raised females
were also lacking laterality. These facts also confirm
the assumption that the group rotational laterality under
new conditions in mosquitofish relates to the sun-compass
orientation (Bisazza and Vallortigara, 1996). Other
authors also relate the laterality in fish motion direction
to migrational orientation (Gleiser, 1981).
Dependence on other factors.
Rotational laterality
depends not only on the sun-compass orientation. In a
work by Bisazza and Vallortigara (1997), the motion of
mosquitofish (
G. holbrooki
) males was studied in a circle
aquaria in the presence of females (or predators).
The females and/or predators were placed under the
transparent cap in the center of the aquarium. In one
variant, the cap was empty. In the presence of the predators,
the males were moving predominantly clockwise.
In the presence of the females, the trend was the
same, although weaker. In the empty aquarium, fish
demonstrated a weak preference of counterclockwise
direction. In this experiment, the aquaria were also lit
from the top by a point source of light. However, dependence
of motion direction on the presence of other fish
indicates that the obtained results cannot be explained
only by the response to a light source. It is likely that,
to track the objects in water, mosquitofish males use
mainly the right eye which results in their clockwise
motion in the presence of other fish.
As was already noted in Section 2, females of mosquitofish
and of some other poecilid and cyprinid fishes
use predominantly the left eye to track their own mirror
reflection (before they get used to it). As a result, in the
aquarium with mirror wall, they move clockwise. However,
this rotational laterality vanishes fast along with
habituation (Sovrano et al., 2001).
Visual reference marks placed along the periphery
of a circle aquarium may suppress the rotational laterality
if these marks stimulate exploratory behavior. If
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black vertical stripes are painted on the aquarium wall,
juvenile Mozambique tilapias (
O. mossambicus
)
actively explore them, turning towards a stripe and
swimming to it from different sides, constantly changing
direction. As a result, laterality peculiar to tilapia
vanishes due to constant changes in direction (Nepomnyashchikh
and Gremyatchikh, 1993).
Perhaps all these results may be due to group laterality
in the use of the right and left eye in different situations.
As was already noted, mosquitofish (
G. holbrooki
) make a detour of a nontransparent obstacle by
the way that the free, not protected by an obstacle
spaces are controlled by a determined eye (Bisazza
et al., 1997b). In a circle aquarium, Mozambique tilapia
(
O. mossambicus
) move mainly along the wall before
they get used to conditions (Nepomnyashchikh and
Gremyatchikh, 1992). It may be assumed that the trend
to move clockwise in tilapia relates to that they check
the internal space of the aquarium mainly by their right
eye. However, this assumption has to be tested.
Individual laterality.
We discussed, above, the
manifestations of rotational laterality under new conditions
for fish. In order to reveal individual rotational laterality,
it is necessary to repeat observations of the same
specimen. If CL sign in repeated experiments will be
the same, then the individual laterality exists. Relevant
observations were carried out on mosquitofish
(
G. hollbrooki
) (Bisazza and Vallortigara, 1996). The
fish caught in the wild were observed in a ring corridor
over five days, 15 min every day. At the first day of
observation, no preferable direction was noted in males
while females exhibited group laterality of motion
(clockwise). Later on, group preference of this direction
vanished. Besides, in the majority of both male and
female specimens, preference for individual direction
(clockwise or counterclockwise) was found, as evidenced
by the correlations of their individual CL values
in repeated trials. The CL correlation between the last
days of observation was higher than between the second
and third days. At the same time, there was no correlation
between the first and latter days. The authors
explain such changes in the mosquitofish behavior by
the presence of two types of rotational laterality in these
fish. One of them, the group laterality, is displayed on
the first day and probably relates to the response to
unknown conditions. The second one, the individual
laterality, is masked at the beginning but then is displayed
and gets stronger along fish habituation to the
experimental conditions.
Similar behavior was observed in goldfish (
Carassius
auratus
; Cyprinidae) juveniles under similar
experimental conditions. At the first day of the experiment,
the group trend to counterclockwise motion was
observed (Nepomnyashchikh, 2005). However, in later
days, this trend had vanished and had been changed by
the individual laterality. As in mosquitofish, the vanishing
of group laterality in gold fish is probably due to
habituation to conditions of the experimental aquarium.
Laterality and fish exploratory behavior.
Fish
explore unknown space and this exploratory behavior
may potentially influence the extent of observed laterality.
First, the motion of fish along the perimeter of the
circle aquarium is interrupted by exploring some of its
parts which is accompanied by frequent changes of
motion direction. These explorations are spontaneous
since they can be observed also in case any of the potential
reference marks are absent in the uniformly lit
aquarium. Such change in motion direction takes place
less frequently in Mozambique tilapia (
O. mossambicus
) (Nepomnyashchikh and Gremyatchikh, 1992)
and more often in goldfish (Nepomnyashchikh, 1998).
At the same time, absolute CL values are higher in tilapia
(Nepomnyashchikh and Gremyatchikh, 1993) than
in goldfish (Nepomnyashchikh, 2005) or, in other
words, laterality in tilapia is more pronounced. It is
clear that frequent change in motion direction may lead
to decrease in laterality. That is why observed differences
between tilapia and goldfish are not necessarily
due to real peculiarities of the CNS asymmetry in these
species. Rather they may result from different intensities
of exploratory behaviors masking the rotational laterality.
Second, both tilapia (Nepomnyashchikh and Gremyatchikh,
1992) and goldfish (Nepomnyashchikh and
Gremyatchikh, 1997) are characterized by a known stability
of motion: the longer the fish moves in a selected
direction (clockwise or counterclockwise) the less is
the probability of its change. This stability is obvious
both while the fish moves in the direction that coincides
with the sign of the group or individual laterality and
the opposite. Mathematic modeling has shown that the
stability of motion results in considerable CL variability
in the “fish” in a model regardless of the fact that the
model stipulates absolutely equal preference of direction
for each specimen. As a result of such variability,
statistically significant differences in CL values (up to
change of the CL sign) may be revealed between the
uniform model “fish” samples if these samples are
small (not more than 20) and the duration of the observations
is short (not more than 15 min). In the experiment
with real goldfish, the same differences of CL values
was observed (Nepomnyashchikh, 2005). This
means that differences in values and sign of group laterality
revealed in the experiments with small groups of
fish belonging to different species or populations do not
necessarily witness real differences in their CNS asymmetries.
Similarly, an observed difference in the individual
CL does not necessarily mean that specimens in
a sample are really different. During the repeating
observations, the CL of these specimens may change
considerably.
Conclusions.
The information given in the present
section allows for the conclusion that the rotational laterality
as well as detouring laterality is not an independent
manifestation of behavioral laterality. It originates
as a result of the interaction of specific experimental
conditions (round aquarium) with responses to various
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NEPOMNYASHCHIKH, IZVEKOV
factors. In particular, the responses to these factors are
determined by the asymmetry in the right and left eye
functions when fish analyze new objects. Hence, group
rotational laterality may vanish after habituation to the
experimental conditions and may be changed by the
individual laterality that has been suppressed under
unknown conditions. As for the individual rotational
laterality, it may result from the asymmetry of eye or
other sense organ functions but in the familiar conditions
as it happens when other experimental methods
are used (see sections 2 and 3). Besides vision, the rotational
laterality may relate to a variety of other functions
of sensory organs on the right and left body sides,
e.g., the lateral line organs. This assumption may be
tested by registering the direction of fish moving in the
dark. However, such experiments had not been carried
out yet.
The rotational laterality may be masked by
responses to visual reference marks, exploration activity
in fish, and by the stability of motion direction even
if this direction does not coincide with the preferable
one. Moreover, the influence of these peculiarities of
fish behavior may lead to the change of sign of the laterality
observed if a relatively small sample of fish was
observed for a short time. Finally, the observed laterality
in some cases may be the result of sun orientation
which has no direct relation to the asymmetry of CNS
or other systems of the organism.
5. Laterality of the Avoidance Response
Group laterality.
An approaching predator or a
sudden strong stimulation cause in fish an avoidance
response: C-bend of the body in the horizontal plane
and lunge leading off the danger. In cyprinids
C. auratus
and
B. rerio
, the group trend to bend right after the
sharp vibration stimulus sensed by the lateral line
organs was revealed. The same trend was revealed in
B. rerio
males and in females when they were chased
by males. In guppy
Poecilia reticulata
(Poeciliidae)
and in four cichlid species, no avoidance response laterality
was observed (Heuts, 1999). During free swimming
in the aquarium when the fish changes direction
spontaneously but not in response to danger, the direction
of turns may differ from that one at the C-bend. For
instance, free swimming
B. rerio
females turn right
more often (as well as when escaping males) but males
turn left more frequently (Heuts, 1999).
In the immature
G. falcatus
, sudden appearance of a
predator model just in front of the fish leads to a predominantly
right turn. If the experiment is repeated
with the interval of seven days, this laterality gradually
changes by the opposite—the fish turn predominantly
left. In a similar experiment, adult specimens at first
exhibit only a weak trend to turn right which changes in
the repeated experiments to a strong trend to left turns
(Cantalupo et al., 1995).
Individual laterality.
Under similar experimental
conditions, other fish (
Jenynsia lineata
; Anablepidae)
do not manifest the avoidance response laterality at a
group level. However, half of the specimens show pronounced
individual laterality as evidenced by a considerable
correlation of individual CL values in repeated
trials (Bisazza et al., 1997a).
Conclusions.
Similar to other types of behavioral
laterality, the avoidance response laterality depends on
the novelty of a stimulus, as well as on the fish species
and sex. At the same time as the opposite to other types
of laterality, it is hard to relate the laterality in response
to vibration stimulus to qualitative differences in the
functions of symmetric sensory organs and analyzers in
CNS. In
C. auratus
, the avoidance response laterality is
manifested much stronger in the case when the fish is
oriented by its head towards the vibration stimulus
compared with the opposite orientation but the laterality
sign does not depend on small (within 20
°
) deviations
of the direction of stimulus action in relation to
the body axis (Heuts, 1999). Besides, the avoidance
response laterality was found in other fish,
G. falcatus
(Bisazza et al., 2005), upon which the vibration stimulus
was directed from below the body. In this case the
direction of C-bend right or left in the horizontal plane
cannot be related to the orientation towards a stimulus.
6. Laterality of Fin Use
In terrestrial vertebrates starting from amphibians,
the laterality in use of extremities is well known (Vallortigara
et al., 1999). Similar laterality in the use of fins
was revealed in some fish. For instance, channel catfish
(
Ictalurus punctatus
; Ictaluridae) use pectoral fins for
stridulation. Some specimens often use fins on both
body sides, while others on one side predominantly,
thus, showing the individual laterality. In the same fish,
the group laterality takes place: most of the specimens
use right-side fins more often (Fine et al., 1996).
Blue gourami (
Trichogaster trichopterus
; Anabantidae)
feel different objects by modified abdominal fins.
During such feeling, gourami use mainly the left fin to
touch plastic or mineral objects while for live objects
symmetrical fins are used with similar frequencies. Perhaps,
in this case, predominant use of the left fin is a
result of eye function asymmetry since gourami prefers
to see an object by the left eye before probing it with a
fin (Bisazza et al., 2001).
CONCLUSIONS
The experimental data show that the laterality in
behavioral responses found in fish relates in most cases
to the functional CNS asymmetry which is also true for
higher vertebrates. This relation is demonstrated in
more detail for responses to visual stimuli. Novelty of a
stimulus to fish, its relation to motivation, and the
extent of the motivation itself, as well as fish sex and
species, determine which one of the symmetrical visual
JOURNAL OF ICHTHYOLOGY
Vol. 46
Suppl. 2
2006
VARIABILITY OF THE BEHAVIORAL LATERALITY IN TELEOSTEI (PISCES) S241
brain centers will dominate the response control. As a
contradiction, the relation of avoidance response to the
CNS functional asymmetry remains uncertain. Perhaps
this relation is due to the asymmetry of the motor system.
Besides, in some fish species, the fin use laterality
is found but it is yet unclear how this relates to the CNS
asymmetry.
As in higher vertebrates in fish of some taxonomic
groups, the laterality at species or population level
(group laterality) was revealed while in others only
individual laterality presents. In some fish species no
laterality was revealed at all. It would be interesting to
attempt to relate these differences to fish phylogeny and
ecology which may allow for understanding of the origin
and adaptive importance of the vertebrate CNS
functional asymmetry. However, in our opinion, not
enough reliable experimental data have been accumulated
yet for such attempts. This is because the variability
of the behavioral laterality due to its dependence on
many factors hampers its study.
In particular, the group laterality is best manifested
in the response to unknown stimulus. Habituation is
accompanied not only by change of sign but in some
cases it leads to the full vanishing of the group laterality.
It can be assumed, for example, that observed differences
in the laterality of responses to visual stimulus
in the fish of different species, age, and sex may be
determined by the rate of their habituation to a stimulus.
Under the same conditions and equal duration of
the observation, it is more difficult to reveal the laterality
in those fish that habituate to the experimental conditions
faster. In Section 4 it was shown how the dependence
of rotational laterality on the peculiarities of
exploration behavior may result in contradictory conclusions
about its size and sign, if theses conclusions
are drawn based upon short experiments with a small
number of specimens. The absence of laterality in such
experiments does not necessarily indicate its real
absence in fish. The same dependence of external manifestations
of the laterality on the peculiarities of fish
behavior may also take place in the case of responses to
visual, vibration, and acoustic stimuli, avoidance
response or fin usage. However, such dependence has
not been studied yet. We believe it is important to
emphasize that, to obtain reliable results, the experimental
methods for studying the behavioral laterality
must be developed with consideration of the speciesspecific
peculiarities of fish behavior.
In conclusion, we would like to note once again that
the present review does not cover the whole material
accumulated by research of the fish behavioral laterality.
To understand its origin and adaptive importance, it
is necessary to reveal the relations between different
types of behavioral laterality as well as the relation of
the latter to the asymmetry of specific CNS sections and
of other systems of an organism. This vast field of
research needs to be reviewed separately.
ACKNOWLEDGMENTS
We are grateful to Angelo Bisazza, Giorgio Vallortigara,
and Boudewijn Heuts for providing us with their
publications and discussions on the present review topics.
This work was supported by the Russian Foundation
for Basic Research, project no. 05-04-48633.
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Translated by D.F. Pavlov