Behavioral Ecology Advance Access originally published online on January 25, 2006
Behavioral Ecology 2006 17(3):358-363; doi:10.1093/beheco/arj040
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Lateralized female topminnows can forage and attend to a harassing male simultaneously
Department of General Psychology, University of Padova, via Venezia 8, I-35131 Padova, Italy
Address correspondence to M. Dadda. E-mail: marco.dadda{at}unipd.it.
Received 3 October 2005; revised 28 November 2005; accepted 15 December 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Animals engaged in a complex task are often unable to allocate enough attention to a second concurrent task. We tested the hypothesis that cerebral lateralization is advantageous because it enables separate and parallel information processing and allows for a more efficient performance of concurrent cognitive tasks. Lateralized and nonlateralized (NL) female Girardinus falcatus, obtained through a selective breeding experiment, were compared in a situation requiring sharing attention between two simultaneous tasks, retrieving food items scattered on the surface, and avoiding unsolicited male mating attempts. In the presence of a sexually harassing male, lateralized females were significantly more efficient than NL females in retrieving food, while no difference between these groups was found in control experiments in which the male was absent and subjects were not required to share attention between foraging and vigilance. Lateralized females showed a negligible decrease in foraging rate while attending the additional task, suggesting that they may be able to partition the two processes in different parts of the brain.
Key words: attention, fish, foraging, harassment, lateralization.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Over the last few decades, the occurrence of functional left-right cerebral asymmetries have been reported in a wide range of animals, both among vertebrates (reviewed in Rogers and Andrew, 2002
) and invertebrates (Ades and Ramires, 2002; Byrne et al., 2002; Pascual et al., 2004), and researchers have begun to speculate about the selective advantages associated with lateralization of cognitive functions (see Vallortigara and Rogers, 2005, for a review of ideas). Empirical evidence for an advantage of lateralized over nonlateralized (NL) individuals has rapidly accumulated and regards species as diverse as fish, birds, and primates (Bisazza and Dadda, 2005; Crow et al., 1998; Güntürkün et al., 2000; McGrew and Marchant, 1999). These studies encompass a broad selection of cognitive tasks, from schooling performance in fish and visual discrimination in pigeons to termite fishing in chimpanzees, and until recently there have been few attempts to produce testable hypothesis about the way functional cerebral asymmetries may improve neural efficiency.
Research on humans, fish, birds, and spiders indicates that subjects that pay attention to one task are often unable to allocate enough attention to an additional task (Dukas and Kamil, 2000; Hebets, 2005; Kastner and Ungerleider, 2000; Metcalfe et al., 1987). Rogers (2000, 2002) has suggested that one of the reasons functional asymmetries are so widespread is that they improve individual ability to cope with divided attention. In her view, lateralization increases the brain's capacity to carry out simultaneous processing by channeling different types of information into the two separate halves of the brain and by enabling separate and parallel processing to take place in the two hemispheres.
Two recent studies conducted on fish and chicks support this hypothesis. Chicks incubated in the dark during the final days before hatching show a poor visual lateralization (Rogers, 1996). Rogers et al. (2004) studied normally and poorly lateralized chicks that had to learn to discriminate between food and nonfood while a model of an avian predator was moved overhead. Lateralized chicks learned faster and were more responsive to the model predator. In control experiment without the predator, no difference in learning ability was found (Rogers, 2000; Rogers et al., 2004).
Dadda and Bisazza (2005) did a similar experiment in the teleost fish Girardinus falcatus. They compare fish from lines selected for high and low degree of laterality in a situation that requires the sharing of attention between two simultaneous tasks, prey capture and predator vigilance. Food-deprived individuals entered a compartment adjacent to the home tank to capture live brine shrimps either in the presence or absence of a live predator at some distance. With the predator visible, lateralized fish were twice as fast at catching shrimps, while no difference in capture rate was recorded when subjects were not required to share attention between vigilance and prey capture.
A weakness shared by the two studies is that they were unable to exclude the possibility that lateralized and NL individuals differed in other traits, for example, their emotional reaction to a dangerous situation. Indeed, recent research has shown that individuals within a population may differ in their antipredator behavior (Brodie and Russel, 1999; Brown and Braithwaite, 2004). These differences are thought to be part of broader differences in "coping styles" or "personalities" such as the shy-bold dimension (Gosling, 2001; Wilson et al., 1994), which appear to have in many cases a genetic basis (Huntingford et al., 1994; Van Oers et al., 2004). Differences in antipredator behavior could have arose as a consequence of different prenatal exposure to light in chicks and particularly in the fish study as a consequence of artificial selection because the test used for measuring lateralization involved predator avoidance behavior (Bisazza et al., 2001).
In this study, we investigated the influence of cerebral lateralization on the management of limited attentional resources employing a dual task that did not involve a response to predators. Specifically, we examined the female's ability to find food while distracted by unwanted mating attempts from a harassing male.
Males of poeciliids, a group of internally fertilizing fish, are among the most ardent in the animal kingdom, their sexual activity being so intense that it can reach one sexual act per minute (Bisazza et al., 1996; Houde, 1997). In contrast, females can store sperm for months, and few copulations are needed to ensure the fertilization of all their eggs for the whole breeding season. The intense sexual activity of males bears several potential costs to the female, the most widely studied being the interference with female's foraging efficiency (Griffiths, 1996; Magurran and Seghers, 1994a,b; Schlupp et al., 2001). In some species, such as Gambusia holbrooki and G. falcatus, males do not court females, and all copulations are achieved through gonopodial thrusting, a form of coercive mating (Bisazza, 1993; Farr, 1989). In these species, male sexual harassment is even more exasperate and can halve female's foraging efficiency (Pilastro et al., 2003). The male in these species is small and inconspicuous and typically approaches the female from behind trying to reach unseen her side and insert its copulatory organ into the female gonopore. Avoiding sneak copulatory attempts requires females to focus attention on approaching males and continuously adjust their position to evade them (Bisazza, 1993; Pilastro et al., 1997).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Subjects
Fish used in this study were males and females of goldbelly topminnow, G. falcatus (Teleostei, Poeciliidae). All females were gravid but not close to parturition. We compared three groups of fish obtained through selective breeding for different degree and direction of lateralization (Bisazza et al., 2001
; Vallortigara and Bisazza, 2002). A stock population of G. falcatus was maintained in our laboratory since 1992 and bred in population tanks. Selection lines were started in 1997 and 1998. Selection was based on scores in the "detour test." The procedure of the detour test has been described in detail elsewhere (Bisazza et al., 2001). Briefly, the apparatus consisted of a large tank with a swimway in the middle allowing the fish inside to face, at both ends of the swimway, a vertical bar barrier behind which the visual stimulus was located. The visual stimulus consisted of a dummy predator, a fish lure used for open sea fishing. The fish was gently pushed using a pair of fishnets at the starting point of the runway. It swam along the runway until it faced the barrier. Ten consecutive trials were given, and we computed the percentage of right and left turns taken by the fish when leaving the runway. The direction taken by a fish is strictly dependent on its eye preference to scrutinize different categories of stimuli (Facchin et al., 1999), and it is highly heritable in this species (Bisazza et al., 2000).
Four populations were selected for the direction of laterality (two replicate populations for left turning and two for right turning), and one population was selected for low laterality (equal preference to turn left or right). All five populations showed significant response to selection when compared with a control line (Vallortigara and Bisazza, 2002). Contrasted in other lateralized tasks, fish of right detour (RD) and left detour (LD) lines tend to obtain opposite scores, and it was suggested that they have a complete mirror-reversed organization of cerebral functions, while NL fish have a bilateral representation of most cognitive functions (Bisazza et al. 2001, 2005; Facchin et al., 1999).
We used adult fish (approximately 6- to 8-months old) from the selection experiments after they had produced their second litter (mostly from generations five and six). Subjects were subdivided into three groups: fish that turned 80% or more leftward (LD group), fish that turned 80% or more rightward (RD group), and fish that turned 50% of times in each direction (NL group). Individuals were maintained in small heterosexual groups (12–15 fish, approximately 1:1 sex ratio) of the same laterality and kept in 70-l glass aquaria with abundant vegetation (Ceratophillum sp.) and 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. Individuals were used once.
Experiment 1
For this experiment, 15 LD, 17 RD, and 16 NL adult females were used. Twenty-two (7 RD, 8 LD, and 7 NL) adult males were used in the tests with male present. Prior to the test, each group of females was maintained for 2 weeks in glass aquaria that were replicas of the test apparatus in order to acclimate the subjects to the novel environment. In every aquarium two adult males with the same direction of lateralization of the females were also present. Groups of adult males were maintained in the same condition. During this period females were partially food deprived: only 30% of the normal food ration was given (except for the weekend when fish were fed ad libitum with A. salina nauplii). Contrarily, experimental males were fed ad libitum during the whole period to ensure that food flakes did not attract them during the test.
The apparatus was similar to that used in a previous study with G. holbrooki (Pilastro et al., 2003) and consisted of an aquarium (60 x 35 cm and 40 cm high with gravel on the bottom), illuminated by two 15-W fluorescent lights and with water maintained at 25 ± °C. Five equally spaced plastic barriers (11 x 40 cm) simulated the plants in the natural environment. Each barrier was composed of a series of elongated bars 1 cm wide and 0.5 cm apart. In this way, the aquarium was virtually divided into six identical sectors. The apparatus was placed in a quiet darkened room and surrounded with a gray nylon net, which acted as a one-way screen to prevent the fish from seeing the observer.
In this experiment, the apparatus was closed with a black plastic cover with a central fissure parallel to the long side of the aquarium to allow the food release. A camera was placed 1 m frontally to the apparatus.
A female was introduced to the apparatus 20 min before the test started. After this period, 10 pieces of food flakes were released on the water surface. Food flakes were small squares (1 x 1 mm) cut from dry fish food (sera GVG-mix). The 10 pieces of food were placed on a plastic sheet (70 x 2.5 cm) at equal distances. The sheet was turned upside down, and the food flakes were scattered on the six sectors (one flake each on the two end sectors and two flakes each on others). The time count began when the female found the fist piece of food and ended when the female ate the eighth of 10 food pieces.
Eight LD, nine RD, and nine NL females were tested alone, while seven LD, eight RD, and seven NL females were tested in the presence of an active male. In the latter condition, an adult male with the same laterality type as the female was inserted in the apparatus 10 min after the introduction of the female. The male was female deprived for at least 7 days before the test and was fed to satiation shortly before being moved to the test apparatus. The test began only if male's sexual activity was intense (at least two attempts per minute). In the few cases in which the male took a food item, the test was terminated and excluded from the analyses.
As we discovered at its end, in this experiment the glass walls surrounded with the gray net created a mirror effect inside the tank. Sometime during the experiment a female left the surface and swam up and down along the wall in an apparent attempt to reach a companion. This behavior was probably related to the fact that females can find relief from male disturbance by shoaling with other females (Dadda et al., 2005; Pilastro et al., 2003). We excluded from analyses the time spent by the female far from the water surface showing this behavior.
Experiment 2
In the first experiment, we could not exclude that the laterality type of males influenced female foraging efficiency. Unpublished data suggest that lateralized and NL males may differ in their mating efficiency. We repeated the experiment using the same type of male stimulus with females of all laterality types. In addition, the apparatus was modified in order to prevent the mirror effect inside the tank observed with the previous procedure.
For this experiment, 12 lateralized females (eight RD and four LD) and 12 NL females were used. In all tests, males from the NL line were used as stimulus. The apparatus used for the first experiment was modified by placing the gray nylon net inside the tank glued against the walls. This allowed us to observe the experiment without disturbance but prevented the fish from seeing its own mirror image. In the second experiment, females were not observed to swim along the wall. A camera was mounted 1 m above the apparatus, and in order to improve the subject's visibility during the recordings, a green plastic sheet was placed on the bottom of the aquarium. In the test with the male present, a second camera was placed in front of the apparatus in order to measure the number of the male's mating attempts and their outcome.
Video recordings were examined by an expert observer, blind with respect to the direction of lateralization of the female. The number of copulatory attempts was recorded from the beginning of the experiment to the moment the female ate the eighth food piece. The outcome of each copulatory attempt was scored, and the proportion of copulatory attempts that ended with a contact between genitalia was computed for each trial. In a closely related species, G. holbrooki, it was shown that this method provides a good approximation of actual fertilization success (Evans et al., 2003; Pilastro et al., 1997).
Statistics were conducted using SPSS 11.5.1. In all ANOVAs, we tested data for normality and homogeneity of variance, and where necessary, appropriate transformation of the data was used.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Experiment 1
Data were analyzed using a two-way ANOVA with laterality type and presence/absence of the male as independent factors. As a dependent variable we considered the average time to retrieve one food item. There is no significant difference in the time spent to retrieve the food between the two groups of lateralized subjects (RD: 12.31 ± 4.43 s, LD: 11.25 ± 4.08 s; F(1,32) = 0.588, ns). The factor presence/absence of the male (F(1,32) = 0.911, ns) and the interaction between the two factors (F(1,32) = 1.048, ns) are not significant. For the subsequent analysis, data from the RD and LD fish were pooled together (hereafter referred to as LAT [lateralized]).
LAT fish were more efficient in foraging behavior than NL fish (F(1,48) = 7.677, p = .008; Figure 1). On the whole, no significant difference due to the presence/absence of the male was found (F(1,48) = 2.680, ns), but the interaction between the two factors was statistically significant (F(1,48) = 6.422, p = .015).
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Observation of Figure 1 suggests that the presence of an active male reduces the foraging efficiency in NL but not in LAT females. We performed a post hoc, paired comparison to verify this hypothesis. When the male was absent there was no significant difference between LAT and NL in the time spent to retrieve the food (t(24) = 0.193, ns), while LAT performed better than NL when the male was present (t(20) = 3.274, p = .004). The performance in LAT female did not significantly differ in the presence or absence of males (t(10) = 0.896, ns), while the difference was marginally nonsignificant in NL females (t(10) = 2.069, p = .058).
There was no significant difference between LAT and NL fish in the time not directly spent to retrieve the food (back and forth along the wall) (F(1,44) = 2.909, ns). Nonetheless, to exclude that removal of the time away from the surface influenced the results, analyses were repeated on total time. No significant difference was found between RD and LD fish (F(1,32) = 2.056, ns; presence/absence of the male: F(1,32) = 1.432, ns; interaction: F(1,32) = 0.421, ns). LAT females foraged more efficiently than NL females (LAT: 17.85 ± 15.26 s, NL: 33.26 ± 24.78 s; F(1,48) = 6.984, p = .011; presence/absence of the male: F(1,48) = 0.073, ns; interaction: F(1,48) = 0.763, ns). LAT and NL subjects did not differ in the time spent to retrieve the food when the male was absent (t(24) = 1.094, ns), while LAT performed better than NL when the male was present (t(20) = 3.535, p = .002).
Sexual activity, measured in percentage of time spent by the male within three body lengths from the female, did not significantly differ between LAT and NL males (RD and LD: 90.8 ± 14.8%, NL: 96 ± 20.8%; t = 0.9, ns).
Experiment 2
There was no significant difference in the time spent to retrieve food between the two groups of LAT subjects (RD: 14.57 ± 2.93 s, LD: 11.35 ± 4.19 s; F(1,8) = 0.40, ns). The factor presence/absence of the male (F(1,8) = 0.024, ns) and the interaction between the two factors (F(1,32) = 0.044, ns) was not significant.
LAT fish were more efficient than NL fish in foraging behavior (F(1,20) = 8.12, p = .010) (Figure 1). No significant difference due to the presence/absence of the male was found (F(1,48) = 2.680, ns), while the interaction between the two independent factors was significant (F(1,20) = 5.64, p = .028).
No significant difference in the time spent to retrieve the food between LAT and NL fish was found when the male was absent (t = 0.270, ns), while LAT fish spent significantly less time than NL females to retrieve food when the male was present (t = 5.394, p < .001). The performance of LAT females did not significantly differ in the presence or absence of males (t(10) = 0.260, ns), while the difference was significant among NL females (t(10) = 3.983, p = .003).
The number of male's mating attempts did not differ significantly in the tests with LAT and NL females (LAT: 6.94 ± 3.29 s, NL: 5.34 ± 1.42; t(10) = 1.092, ns). The proportion of copulatory attempts that ended with contact between genitalia did not differ significantly in the tests with LAT and NL females (LAT: 0.222 ± 0.043, NL: 0.187 ± 0.029; t(10) = 0.66, ns), although in the first 2 min of the test, when male activity was very intense, we observed a trend toward a large proportion of genitalia contact in NL females (LAT: 0.128 ± 0.038, NL: 0.248 ± 0.039; t(10) = 2.89, p = .053)
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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LAT females G. falcatus were more efficient than NL females in retrieving food items when tested in the presence of a distracting task, namely, avoiding unwanted copulatory attempts from a sexually active conspecific male. In control groups without a male present, no difference in food retrieving was found between these two laterality types. Male sexual activity did not differ among laterality groups, and the difference between LAT and NL females was observed both in the first experiment, when male and female were of the same laterality, and in the second experiment, where the same type of male was used for all tests. We found no indication that the proportion of successful male copulation was larger with LAT females, and, rather, in the second experiment, we observed a nearly significant trend toward a better ability of LAT females to avoid unwanted copulations. This seems to exclude the possibility that LAT females were more often unaware of male presence or that NL and LAT females displayed different trade-offs between retrieving food and avoiding unwanted copulation, that is, LAT females were able to increase their efficiency in retrieving food by reducing the attention toward the harassing male.
A lack of a significant difference in the proportion of successful male copulation also allowed us to exclude the possibility that NL and LAT females displayed different trade-offs between retrieving food and avoiding unwanted copulation, that is, LAT females were able to increase their efficiency in retrieving food by reducing the attention toward the harassing male.
These findings parallel those obtained in previous studies with G. falcatus and chicks showing a better performance of LAT subject in a dual task that consisted for both species in foraging and displaying antipredator behavior concurrently (Dadda and Bisazza, 2005; Rogers et al., 2004). Because no predator response was involved in the present study, we can safely conclude that a better management of attentional resources and not a difference in boldness or other coping styles explains a better efficiency of LAT individuals in concurrent tasks.
Our study evidenced little difference in performance between individuals lateralized in opposite directions. This is in agreement with previous finding, indicating a similar performance and suggesting mirror-reversed behavioral lateralization in lines selected in opposite directions (Bisazza and Dadda, 2005; Bisazza et al., 2001, 2005; Dadda and Bisazza, 2005). It is interesting that a similar situation has been described in humans. Crow et al. (1998) reported that in verbal tests conducted in a large sample of 11-year-old children, strongly left- and right-handed individuals had similar scores, and both performed slightly better than ambidextral individuals.
In the present study, NL females were found to halve their efficiency to find food when required to perform a concurrent demanding task, avoiding male copulations, while LAT females appeared little affected by the presence of the male. The other study investigating dual performance in G. falcatus (Dadda and Bisazza, 2005) provided information about the proximate mechanisms that allow a more efficient management of attentional resources by LAT fish. LAT fish were found to monitor the predator with one eye (the eye was different for LD and RD fish) and to use the other eye for catching prey, whereas NL fish swapped between tasks using each eye for both functions. This suggests that in LAT fish, different types of information might be effectively channeled into the two separate halves of the brain thus enabling distinct and parallel processing to take place in the two hemispheres.
Reciprocal interference between simultaneous tasks has been widely investigated in humans, and it appears to operate also across sensory modalities (Kastner and Ungerleider, 2000; Rapp and Hendel, 2003; Spence et al., 2001). Behavioral studies revealed that animals are constrained in the amount of attention that can be simultaneously focused on different activities and that individuals attending to one task often suffer a reduced efficiency in other tasks. A trade-off of attentional resources during simultaneous accomplishment of foraging and vigilance was documented in both fish and birds (Dukas and Kamil, 2000; Metcalfe et al., 1987). This cognitive limitation may have a large impact on an individual's fitness. For example, guppies catching live Dapnia were captured more often by a predator when the density of Dapnia increased (Godin and Smith, 1988). Similarly, female wolf spiders are less likely to notice a predatory visual stimulus and hence get caught more often when exposed to a courtship vibration emitted by a male (Hebets, 2005).
The advantage of better management of attentional resources is evident also in the situation studied here. G. falcatus, as with other topminnows, feed largely on small insects falling onto the water surface. Females are viviparous and reproduce continuously during a breeding season that may last the whole year in tropical zones. To reproduce, they need large amounts of energy, and the continuous sexual harassment from males may severely reduce their food intake. In the closely related western mosquito fish, the presence of a male can halve female foraging efficiency (Pilastro et al., 2003). Even if females have evolved a number of strategies to reduce these costs, including promoting male-male fights or diluting male disturbances by joining other females (Dadda et al., 2005), costs on reproductive fitness may remain high. In this context, lateralization appears extremely advantageous because it allows a female to continue to gather the same quantity of food even when she is involved in avoidance of frequent male sneaky copulatory attempts.
In their natural environment, in addition to finding food and avoiding males, females have to accomplish several other cognitive tasks. For example, they must monitor the environment for the presence of predators, orient themselves in the space, and coordinate their movements with other schoolmates (Brown, 2005; Brown et al., 2004). Because many of these activities compete for the same attentional resources, the impact of cerebral lateralization on survival and reproduction may be even larger than highlighted in this study.
Although the results of this and two previous studies point to a significant role of lateralization in the management of attentional resources, this is probably not the sole advantage that explains the pervasive presence of lateralization in the animal kingdom. Güntürkün et al. (2000) described an advantage of LAT pigeons in learning a discrimination between food and nonfood, and Crow et al. (1998) in a study on 13-year-old boys and girls report slightly better verbal and mathematical abilities in individuals with marked lateralization. Both situations do not seem to imply dividing attention among concurrent tasks. Two recent studies in G. falcatus also showed an advantage of LAT individuals in situations that apparently do not involve limitations due to divided attention. In one study, LAT fish proved better than NL fish in using the geometry or the salient feature of the environment to reorient themselves in space (Sovrano et al., 2005); in the other study, schools of LAT fish moving in a novel environment showed significantly more cohesion and coordination than schools of NL fish, and in mixed schools, LAT fish occupied more often the center, a position associated with the reduction of predation risk and energy expenditure (Bisazza and Dadda, 2005).
Counter to the view of a generalized superiority of a specialized brain, LAT animals might have costs to pay. Some authors have suggested that in LAT animals, advantages provided by enhanced cognitive capacity and efficiency of the brain might be counteracted by ecological disadvantages of lateral biases in behavior (Vallortigara and Rogers, 2005). Common toads, for instance, are more likely to strike at a prey when it moves in their right monocular field than when it moves in their left monocular field (Vallortigara et al., 1998). By contrast, three species of toads were found to react more promptly when a predator was seen in their left monocular field (Lippolis et al., 2002), a result that has recently been replicated in a marsupial species, the dunnarts (Lippolis et al., 2005). Toads, lizards, and gelada baboons direct more aggressive responses to conspecifics on their left side than on their right side (Deckel, 1995; Hews et al., 2003; Vallortigara et al., 1998). Because the outside world is largely unbiased, perceptual and motor systems that are asymmetrical might generate handicap, for instance, leaving an animal more vulnerable to predation on one side, unable to catch some of the available prey, or exposed to competitors that have learned to exploit its side biases. The confirmation of such trade-off could clarify why substantial variability in the degree of lateralization is maintained within populations in spite of the broad evidence that lateralization enhances the efficiency of neural operations.
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ACKNOWLEDGEMENTS |
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We thank Jamie L. Russell and Culum Brown for their helpful comments and Simone Dalla Chiara and Paola Pezzin for their help with the experiments. This work was supported by research grants from Ministero dell'Università, dell'Istruzione e della Ricerca and University of Padova to A.B.
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