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Lateralization in manatees BEHAVIORAL LATERALIZATION IN THE FLORIDA MANATEE ( TRICHECHUS MANATUS LATIROSTRIS ) BY KARA TYLER A Thesis Submitted to the Division of Social Sciences New College of Florida in partial fulfillment of the requirements for the degree Bachelor of Ar ts Under the sponsorship of Dr. Gordon B. Bauer Sarasota, Florida April, 2009
Lateralization in manatees ii Acknowledgements Special thanks to the United States Fish and Wildlife Service, Lowry Park Zoo, The Living Seas at Epcot, Mote Marine Laboratory, Parker Mana tee Aquarium, Joseph Gaspard for permitting observations. Dr.Duff Cooper and Dr.William with data collection. Thanks to Dr. Gordon B. Bauer for being a dedicated advisor Finally, a thanks to Paul Julian II for his unwavering love and support.
Lateralization in manatees iii TABLE OF CONTENTS Content Page Number Acknowledgements ii Table of Contents iii Abstract iv Chapter 1. Introduction 1 Chapter 2. Behavioral Pr eferences 14 Chapter 3. Marine Mammals 22 Chapter 4. Evasion Behavior and Scar Data 30 Chapter 5. Manatee Biology and Behavior 37 Method 42 Results 47 Discussion 51 References 57 Tables 66 Figures 68 Appendix A 7 2 Appendix B 73 Appendix C 74 Appendix D 76
Lateralization in manatees iv BEHAVIORAL LATERALIZATION IN THE FLORIDA MANATEE ( TRICHECHUS MANATUS LATIROSTRIS ) Kara Tyler New College of Florida, 2009 ABSTRACT Throughout the lateralization literature many species of ani mals ranging from fishes to primates show population level and individual level behavioral lateralization. This study examined behavioral lateralization in the Florida manatee using observations of 47 wild and 26 captive manatees. Flipper uses were used to determine behavioral lateralization of flipper preferences and scar patterns (N=46) were used to determine lateralization of evasion behavior. Overall for both captive and wild manatees combined, the manatees displayed a tendency to prefer the left flippe r at the population level ( p =0.07). Manatees display different preferences for different tasks, which may be affected by the complexity of the task. Scar data reveal that manatees may avoid boats to the right as significantly more scars were found on the l eft side of the body, indicating a population level bias during evasion behavior and suggesting that manatees may have lateralized brains, at least in terms of the avoidance response. Dr. Gordon B. Bauer Division of Social Sciences
Lateralization in manatees 1 Behavioral Lateraliz ation in the Florida Manatee ( Trichechus manatus latirostris ) Chapter 1. Introduction to Lateralization The two hemispheres of the brain are known throughout the animal kingdom to specialize in different tasks, a phenomenon known as lateralization (Bisazz a, Rogers, &Vallortigara, 1998). Behavioral asymmetries and lateralization of the nervous system may date back as far as trilobites in the Early Cambrian period (Babcock, 1993) and such asymmetries exist in many organisms from fishes to primates. By examin ing limb preferences at both a population (a majority of the population of a species exhibits the same preference) and individual level (the population of a species is approximately equally divided for limb preferences), more can be learned about the brain in a noninvasive manner. Lateralization of the brain has been studied by looking at behavior, particularly limb preferences to such an extent that certain tests have been devised Kong tests for dogs (Batt, Batt, & McGreevy, 2007). The brain is divided into the left and right hemispheres. For a majority of behaviors and functions the contralateral hemisphere controls the limb or sensory system on one side of the body. For example, the left hemisphere controls the right arm (Kalat, 2007). Looking at the preferences of different sides of the body (limbs, eyes) in different contexts and tasks reveals the specializations of each hemisphere that are common throughout the animal kingdom. Research suggests that the left hemisphere is responsible for considered responses, inhibiting responses (such as escape), focusing attention, sequential analysis, inhibiting the right hemisphere, and for feeding and prey capture. Recent research suggests that the right hemisphere is responsible for rapid responses,
Lateralization in manatees 2 unfocused attention, intense emotions, parallel processing, spatial information (maps), and species typical responses such as escape, fear, and aggression (Rogers, 2002). The brain of the man atee is an enigma due to its unusually smooth surface (Reep & Bonde, 2006). Behavioral lateralization may be a useful tool to gain more knowledge the hemispheres of the manatee brain. Throughout the animal kingdom, lateralization and limb preferences exist even in animals with more primitive brains: fin preferences in catfish populations (Bisazza, Rogers, &Vallortigara, 1998); eye preferences of fish for viewing a pr edator (Facchin, Bisazza, & Vallortigara, 1999); forepaw preferences in toads to remove a balloon from the head (Bisazza, Cantalupo, Robins, Rogers, & Vallortigara, 1996); a population turning preference in male newts during mating behavior (Green, 1997); turning preferences in fish during predator evasion (De Santi, Sovrano, Bisazza, & Vallortigara, 2001); and foot preferences at the population level in birds (Harris, 1989). This review will address important topics in lateralization, including theories a bout the origins of lateralization (both genetic and evolutionary), why lateralization arose and why it still exists. The benefits of lateralization such as enhanced multitasking (individuals) and group coordination (populations) will be addressed. Differe nces in preferences across different actions and behaviors have been found in primates and elephants, a relative of the manatees, and these differences will also be discussed to understand why some animals exhibit population level preferences while others do not. Lateralization in other marine mammals and lateralization of scars and evasion behavior
Lateralization in manatees 3 are covered followed by the basic biology and behavior of the Florida manatee. A review of the neuroanatomy of the Florida manatee is presented in Appendix D. O rigins and multitasking essence of brain lateralization lies in the fact that one side of the brain performs certain types of computational operations and the other side pe rforms other, different that the direction of lateralization of the brain is not as important as the presence of different functional specializations of the two hemisph eres. The direction of lateralization may be genetic and is found to be similar among closely related species of fish. The benefit of lateralization may be that the brain performs complex problems better if it segregates them into sub problems. The reason that lateralization arose so early in evolution might have been to solve the problem of functional incompatibility, the problem of the two hemispheres trying to perform the same task or the same hemisphere trying to perform more than one task, and to incre In order to determine whether a lateralized brain really does enhance performance and multitasking in an organism, a researcher needs to have both lateralized and non lateralized subjects of the same species. Findi ng an equal number of subjects that are naturally lateralized and subjects that naturally lack lateralization, or subjects that display opposite preferences to the same degree is not always possible. In some species, however, the side and degree of lateral ization are genetic. Lateralization is genetic in fishes and fishes have shorter breeding cycles than other organisms and therefore, breeding differently lateralized lines of fishes is fairly easy and quick. For these reasons,
Lateralization in manatees 4 a large proportion of the lit erature on the benefits of lateralization has used fishes as subjects with other species and phyla being poorly represented. A few of these experiments using fishes provide evidence that lateralization of the brain is indeed beneficial to an animal through enhancing performance and multitasking abilities. Sovrano, Dadda, & Bisazza (2005) investigated whether lateralization in fish is associated with better performance in spatial tasks. The researchers tested female Goldbelly topminnows ( Girardinus falcatus ) that were specially bred for direction of lateralization against females that were bred to be non lateralized in a task requiring the use of geometric and non geometric cues (to find an escape door). All fish learned to reorient to the door after a 90 r otation of the tank, however the lateralized fish learned sooner than the non lateralized fish. The non lateralized fish had difficulty using geographical information to distinguish between the two corners with the same geometrical cues, which they frequen tly confused. In a second experiment only non geometric cues were available and both groups learned the task. The lateralized females learned the task with fewer trials and errors and they learned it significantly sooner than non lateralized females. The results imply that non lateralized fish have trouble using both non geometrical and geometrical cues possibly due to a lower ability to simultaneously process dual information stemming from a non lateralized brain (Sovrano, Dadda, & Bisazza, 2005). Later alization also enhances the ability of fish to feed and attend to a predator simultaneously (Dadda, & Bisazza, 2006a). The researchers tested three groups of Goldbelly topminnows selectively bred for different directions of laterality (right, left, and non e). They tested an experimental group in the presence of a predator (in a separate
Lateralization in manatees 5 tank next to the feeding tank), a male pumpkinseed sunfish, and a control group without a predator present. The experimenters recorded the amount of time needed to capture 1 0 nauplii (brine shrimp), the number of nauplii caught on the left or right side of the fish and the eye used to watch the predator during the test. The presence of the predator increased the time needed to capture nauplii. The lateralized fish caught sh rimp faster than the non lateralized fish and the capture time of the lateralized fish changed only slightly in the presence of the predator, but doubled in the presence of the predator in the non lateralized fish. This suggests that the non lateralized su bjects divide their time and attention between watching the predator and capturing prey. When the predator was absent the groups did not differ in their ability to capture shrimp, however, in the presence of the predator the lateralized fish were more effi cient at capturing shrimp than the non lateralized fish. In the absence of the predator, the lateralized fish caught shrimp with an equal frequency on either side of the body, but in the presence of a predator the left lateralized fish caught more shrimp o n the left side of their body and watched the predator with their right eye. The right lateralized fish caught more shrimp on the right side of their body and watched the predator with the left eye. The non lateralized fish did not display a side differenc e. The results suggest that the lateralized fish used one eye and hemisphere to monitor the predator while the other eye and hemisphere were free to watch and capture prey. Lateralization may also be beneficial to female topminnows allowing them to forage efficiently despite being distracted by a harassing male (Dadda, & Bisazza, 2006b). Dadda and Bisazza tested female topminnows bred for lateralization as well as non lateralized females in a task in which females had to avoid unsolicited mating
Lateralization in manatees 6 attempts f rom males while trying to forage. Lateralized females were far more efficient at foraging than non lateralized females. The presence of the distracting male reduced the foraging efficiency of the non lateralized females but not the lateralized females. In the presence of males, the females differed in the length of foraging time needed with the lateralized females foraging faster. These results suggest that lateralization may improve multitasking and that it may increase the fitness of the females who are l ateralized despite the possible vulnerability to predators that may occur on one side when a fish is lateralized (Dadda, & Bisazza, 2006b). Behavioral asymmetries are clearly advantageous at an individual level, however, these asymmetries could be disadva ntageous at the population level if predators learn the bias of their prey and use it to their own advantage. In such a case an individual level asymmetry could be better for the benefits of a lateralized brain without predictable behavior at the first enc ounter. Sociality of species may have provided the pressure to develop population level lateralization. A species is social if the animals live in a structured group (Pough, Janis & Heiser, 2005). All species of social fish that were examined by the resear chers were lateralized at the population level, but not the solitary species of fish. This may be beneficial in social fishes to keep a school of fish together (Vallortigara, Rogers, & Bisazza, 1999). Based on these observations by Vallortigara et al., it is possible that an intermediate species would show an intermediate bias, not a strong population bias, but somewhere closer to population level than evenly split. Manatees, as an example, are normally found alone or with a few other manatees with the exce ption of the winter months when they are found in large congregations of individuals while seeking refuge in warm water sites. As the manatees display such an intermediate
Lateralization in manatees 7 form of social behavior and can be categorized as a semisocial species (Reynolds, 19 79), they would be expected to display an intermediate bias. Social basis Unlike the clear benefits of individual lateralization mentioned above, population level biases have ambiguous benefits as well as many costs. Asymmetrical systems are vulnerable to attack on their preferential side or are at a disadvantage to attack prey or competitors appearing on the non dominant side. However, the advantages associated with an asymmetric brain can counteract the ecological disadvantages of behavioral asymmetries. One of the advantages of lateralization is increased neural capacity because by specializing one hemisphere for a particular function it frees up the other hemisphere to perform other functions. Doing this avoids the duplication of functions in both hemis pheres and spares neural tissue. Additionally, the specialization of one side of the brain prevents simultaneous initiation of incompatible responses in organisms with carry out simultaneous processing by enabling parallel processing. All of these are very strong benefits, but still do not explain population level lateralization. Individual lateralization would, therefore, be more beneficial for a solitary animal than po pulation lateralization. A population level bias common for most individuals could be an evolutionarily stable strategy when individually asymmetric animals live socially and coordinate their behavior with others (Vallortigara, 2006). Vallortigara formal ized a game theory model indicating that lateralization at the population level can be evolutionarily stable. Prey predator interaction was incorporated into the model and indicated that for small groups of solitary prey the only stable
Lateralization in manatees 8 population consists of equal proportions of left and right preferent individuals, if one preference were more prevalent the predators of that species would learn to predict certain behaviors and individuals possessing the more common preference would be killed more easily an d at a higher rate, bringing the prevalence of the preference down. Stable populations for larger groups would consist of unequal proportions of left and right preferent prey. For the population this would mean that the majority would gain protection (as i n the case of schooling fish) but there is a cost of vulnerability to predators. The minority of individuals that are lateralized in the other direction would get the trade off of the protection of the group with low predictability of their behavior for pr edators. Formal experiments done using fish indicate that species that shoal are lateralized at the population level and the solitary species were mostly lateralized at the individual level (Vallortigara, 2006). At least six species of social fish exhibit population level lateralization. In a set of two experiments, Sovrano, Rainoldi, Bisazza, & Vallortigara (1999) first examined preferential use of the eyes during viewing of mirror images in mosquitofish ( Gambusia holbrooki ) and redtail splitfins ( Xenoto ca eiseni ). The males of these two species do not usually school and typically avoid each other and are not known to show a bias for viewing mirror images. For this reason, the researchers used females and males maintained in the laboratory with the additi on of recently wild caught male mosquitofish and laboratory raised redtails The researchers tested the fish individually in a tank with mirrors for the two longer walls and opaque screens as the two shorter walls. Eye use was determined from the angle of was a significant bias overall for left eye use in females of both species, no significant
Lateralization in manatees 9 bias for eye use in the habituated males, and the recently caught males differed significantly from the habituated males by possessing a significant bias overall, but not from the females suggesting that male G. holbrooki have a tendency to show schooling behavior (as shown by behavior similar to females) when in a novel environment. In the second experime nt, the experimenters examined four other fish species to determine if the directional asymmetry is invariant using angelfish ( Pterophllum scalare ), Eurasion minnows ( Phoxinus phoxinus ), female blue gouramis ( Trichogaster trichopterus ), and Sarasins minnow s ( Xenopoecilus sarasinorum ). The fish were all tested in the same apparatus using the same method as the first experiment. All of the fish showed a strong preference to use the left eye to view the nearest mirror except for the blue gourami, which did sho w a strong preference for the left eye to view the distant mirror image rather than the closer one (Sovrano, Rainoldi, Bisazza, & Vallortigara 1999). The common preference for the left eye to view the mirror image in all six of these widespread species su ggests that the left eye bias indicates right hemisphere specialization to view conspecifics in many fish and may be the evolutionary precursor to lateralization in later vertebrates. This study gives evidence in support of the theory that population level lateralization is beneficial to social species, such as the previously mentioned fish which are schooling species. Population level lateralization is absent in another species of fish, a solitary species. Males of a domesticated fish species, Betta sple ndens do not exhibit a population level asymmetry, but do exhibit lateralization at the individual level (Cantalupo, Bisazza, & Vallortigara, 1996). The experimenters placed males into a tank with a mirror at the bottom and recorded the number of left and right lateral displays
Lateralization in manatees 10 made to their mirror images. The fish did not display a population level bias, however there was a significant correlation between the numbers of lateral displays, total duration and mean duration of displays, suggesting that these fish do display an individual bias in eye use. In a second experiment using the same fish the mirror was removed and instead a female was placed in the center in a glass tube. Once again the fish did not display a population level bias, and all three measu res were correlated between trials. For those fish that were in both experiments, there was a positive correlation between the data obtained in both experiments suggesting that eye preference is constant across time and situations for individuals. Individu al lateralization could still imply beneficial brain lateralization if the direction of lateralization does not matter for the brain to function efficiently and if it does need to be lateralized to do so. Bettas do not school and are mostly solitary fish, their lack of population level lateralization supports the theory that population biases are only found in and beneficial to those species that are social. While adult anurans may not be social, during their tadpole stage they live in large congregations that may be considered social and even display population level turning preferences during this stage (Wassersug, Naitoh, Yamashita, 1999; Bisazza, De Santi, Bonso, Sovrano, 2002). Behavioral asymmetries also exist at the population level during social beh aviors in the smooth newt. Green (1997) recorded courtship behavior between groups of two males and one female smooth newt and found that males displayed a bias of turning to the left during creep on (phase of courtship behavior) than to the right or no bi as. While newts may or may not be viewed as a social animal, the presence of a population level turning preference during a social behavior (courtship)
Lateralization in manatees 11 population le vel in social contexts in which animals need to coordinate behavior. Cottonmouths, a solitary reptile, do not display a population level bias for non social coiling behavior (Roth, 2003). Tortoises may be considered semisocial in that they can live togeth er peacefully in large groups, whereas they may not live in structured groups in the wild, similar to the social behavior of manatees when they are found in large congregations at warm water sites during the winter months. Tortoises also show evidence of l ateralization at the population level for righting responses (Stancher, Clara, Regolin, & Vallortigara, 2006). In the first experiment looking at lateralization in the Chelonian order, the researchers tested two subspecies of the Mediterranean tortoise, T. h. spp. hermanni and T. h. spp. boettger In the righting task the researchers turned the tortoises up side down and the tortoises had to turn themselves back right side up. The researchers videotaped the trials and scored each trial for direction of righ ting by recording which hind leg was kept still during the righting procedure. More subjects flipped to the right than to the left. The results give supporting evidence of individual and population level lateralization in the Chelonian order with a signifi cant population level bias to right to the right in this species. However, as these tortoises do not congregate in the wild, this may go against the model for lateralization in social versus nonsocial species. They do not often face the need to cooperate o r coordinate their behavior in any way, but perhaps the bias to right themselves arose for cooperation during courtship or mating behaviors. Parrots are social birds that live in large flocks and most species form pair bonds that last throughout the year (Luescher, 2006). Thirteen species of Amazon Parrots and Macaws display population level preferences for the left foot during feeding behavior
Lateralization in manatees 12 (Friedmann & Davis, 1938), which provides very strong evidence of population lateralization of parrots, a social species. Perhaps the common foot preference enhances the ability of these birds to interact and cooperate within their flocks. Sheep, a social species of mammal, also display population and individual level preferences, in accordance with the theory reg arding population biases. Versace, Morgante, Pulina, & Vallortigara (2007) investigated the preferences of sheep while avoiding an obstacle in order to rejoin conspecifics, the foreleg used to step up onto a wood board and the spontaneous preference in the direction of jaw movement during rumination. The sheep demonstrated a population level preference to avoid the obstacle to the right, but did not display a foot preference. The authors suggested that perhaps the right side population bias for avoiding obj ects might be due to the gregarious behavior of the sheep. It could enhance the ability of a herd to stick together. They also propose that gregarious species may be more likely to show asymmetries in social activities (Versace, Morgante, Pulina, & Vallort igara, 2007). The majority of the studies mentioned above offer evidence that supports theory, however more research needs to be done on other species. Vallortigara mainly mentions species of fish as fitting into this model and very f ew studies have looked into lateralization in reptiles, amphibians, solitary birds and solitary mammals. The Florida manatee is a semisocial species that congregates during the winter at warm water sites (Reynolds, 1979). Additionally, the mother calf re lationship lasts for 2 3 years or longer (Reep & Bonde, 2006). Manatees would be expected to display a weak population
Lateralization in manatees 13 theory model. However, manatees are very rarely preyed upon and therefore might not be subject to the same selection pressures for lateralization as other species are.
Lateralization in manatees 14 Chapter 2. Behavioral Preferences Limb Preferences and Task complexity Another theory exists to attempt to explain the presence or absence of limb preferences in an organism, the theory of task complexity. This theory suggests that tasks that require more skill or manipulation would show stronger preferences whereas either limb can perform more simple tasks equally. The theory of tas k complexity also suggests that more complex (high level) and/or bimanual actions would be more likely to reveal a population level preference (Fagot & Vauclair, 1991). Several studies using chimpanzees offer results in support of the theory of task comple xity (Hopkins, 2006; Chapelain, Bec, & Blois Heulin, 2006; Vauclair, Meguerditchian, & Hopkins, 2005). Primates use their limbs (hands) to manipulate food items and show a preference for one hand at the population level and this preference is affected by the complexity of the action. Hopkins (2006) evaluated the distribution of handedness across great apes in published and unpublished reports since 1990 using a common handedness index. The primates displayed a population level right handedness. There were also more strongly right handed than strongly left handed subjects. Bonobos had the highest percentage of right handed subjects followed by gorillas and chimpanzees, which had significantly higher percentages of right handed subjects than orangutans, of wh ich there were more left handed subjects. The testing environment was significantly correlated with the left handed subjects, however there were more strongly right hande d than strongly left handed subjects in captivity. Task specificity was found for hand use, with population level right handedness occurring for actions such as leading limb during locomotion,
Lateralization in manatees 15 grooming, feeding, throwing and the tube task. There was a left handed population bias for actions such as carrying, holding, and termite fishing. Hopkins pointed out that small sample sizes, differences in measures used to calculate handedness, and differences in task complexity may be the cause of discrepancies be tween the many studies on handedness in primates and the lack of significant population biases reported in many of the published studies. Supporting this, the more complex and bimanual actions were more highly lateralized than unimanual actions, and the mo st common behaviors did not show strong individual or population level biases suggesting that the more rare and complex actions should be used for measures of handedness. Hopkins (2006) suggests that there is a possibility for much stronger population and individual level biases if more sensitive measures are used. Fagot and Vauclair (1991) make similar suggestions and observations about handedness in primates and other animals. The authors examined many previous studies on handedness in primates, 48 studi es involving food reaching tasks and 28 studies of primates tested in an open space with no movement constraint on reaching. Of the 48 studies, three showed a tendency (probability less than 0.10) for a left hand bias, one showed a bias for the right hand, three studies showed a significant left hand bias and the rest did not show any asymmetries. Of the 28 studies without a movement constraint, three studies exhibited a preference for one side, and the remaining 25 studies did not exhibit any significant p opulation level bias. Based on the studies examined, the authors made several explanations for the lack of significant results. The authors suggest that both hands can perform some tasks equally, but one hand or hemisphere would be better at performing mor e difficult tasks. Actions requiring more skill should show stronger
Lateralization in manatees 16 biases, and only high level tasks should reveal hemispheric specialization. Low level tasks will likely not show a group level bias, however, preferences expressed in one low level task c an generalize to other low level tasks. The authors also make note that calculating a side preference over a number of tasks without separating the tasks and calculating them separately could mask any asymmetry that may exist. Initial attempts to perform a highly controlled task are more likely to exhibit asymmetries giving rise through experience to a shift from an asymmetrical to a symmetrical distribution of hand biases at a group level due to the repetition of the task causing both hemispheres to become competent at performing the same task (Fagot & Vauclair, 1991). Although the two previous reviews examined the data from many primate handedness studies and made suggestions about possible confounding factors, neither study actually tested the theory of task complexity and movement constraints. Chapelain, Bec, and Blois Heulin (2006) put the theories to the test. Using observational and experimental paradigms they looked at the effects of posture and task complexity on n the first part of the study they observed 12 monkeys and recorded their hand use during spontaneous feeding. The experimenters recorded which hand was used for feeding, what the other hand was doing at the time and the posture of the monkey. The Handedne ss Index was used to calculate a score for each subject: (R L)/(R+L). During observations the monkeys produced 26 different spontaneous actions, and 21 of the 26 actions induced a significant individual bias. The monkeys displayed a group level bias for th e right hand for two of the actions and three subjects were strongly lateralized for suckling. The monkeys showed a bias at the group
Lateralization in manatees 17 level to use the right hand to perform a main action while the left hand holds a food item with the direction and strength of laterality depending on the secondary action. The experimental procedures consisted of reach tasks with varying posture, and box tasks with varying complexity. In the reach tasks an experimenter presented a seed to the subject in such a way that the s ubject had to adjust its posture in order to reach the seed. The different postures were sitting, standing bipedally, clinging, and standing tripedally. In the box tasks the subject had to open the lid of a box and hold the lid open with one hand while gra bbing a seed from the box with the other hand (complex task) and in the simple task the box did not have a lid and the subject simply needed to reach into the box to grab the seed. None of the experimental tasks revealed group level biases and none of the subjects had a consistent preference, however, five subjects were always lateralized. Posture did not affect the direction of the hand preference, but did affect the strength of the preference, with the strength being weaker for the triped stance. Experime ntal tasks revealed a larger number of lateralized subjects than the spontaneous actions and the preferences were stronger in the experimental actions. This supports the theory of task complexity, that more complex tasks are more likely to reveal hand pref erences, with the box task inducing the strongest preferences and the supposed easy posture (triped stance) inducing the weakest preferences. Although the results are not overwhelming, they do show a trend that supports the theory of task complexity. In a similar study, Vauclair, Meguerditchian, & Hopkins (2005) investigated whether baboons would be more strongly lateralized for bimanual or unimanual tasks, with the bimanual tasks seen as more complex. In the unimanual task the experimenters observed the b aboons to see which hand was used to reach for food while seated. They
Lateralization in manatees 18 also tested the baboons four months later for consistency. In the bimanual task the experimenters gave the baboons a PVC tube filled with peanut butter and observed to see which hand th e baboons used to scrape the peanut butter out while the other hand held the tube. The researchers tested the baboons eight months later to test for consistency. The unimanual task did not produce a population level bias. The bimanual task, on the other h and, produced a population level bias for the right hand. In regards to consistency, only in the bimanual task did the subjects exhibit a consistent preference across time; the unimanual preferences were not consistent. All of the studies with primates previously mentioned support the need to test for laterality using more complex activities, rather than low level manual activities such as reaching which could be biased by other factors. These findings could also have implications for testing preferences in other animals besides primates. I expect manatees to display stronger preferences for more manipulatory actions and for bimanual actions such as feeding and digging in comparison with simpler behaviors such as locomotion, substrate touches and touching other manatees. Limb Preferences Limb preferences are used widely in the literature as a possible indicator of hemispheric lateralization. Although some studies suggest that some form of manipulation is required for an animal to exhibit a preference or lateralization, limb preferences exist for animals that do not use the limbs to manipulate objects and for behaviors that do not accomplish manipulation in animals that do use the limbs to manipulate objects. Researchers have investigated limb preferences in animals that do not use the limbs for manipulation such as fish (Bisazza, Lipolis, & Vallortigara, 2001), frogs
Lateralization in manatees 19 (Bisazza, Cantalupo, Robins, Rogers, & Vallortigara, 1996) and tortoises (Stancher, Clara, Regolin, & Vallortigara, 2006). Researchers have a lso investigated limb preferences for behaviors that do not include manipulations in animals that do have the ability to manipulate objects such as birds (Harris, 1989), primates (Hopkins, 2006), and other mammals (Dolphins: Sakai, Hishii, Takeda, & Kohshi ma, 2006; Rats: Aggestam & Cahusac, 2007; Elephants: Martin & Niemitz, 2003). In one of very few studies on fin preferences in fish, gouramis exhibit evidence of lateralized ventral fin use in exploring objects. Bisazza, Lippolis, & Vallortigara (2001) t ested fish separately in a tank in which different objects were placed and recorded the first ventral fin used to contact the objects (in the first experiment) and the first three contacts (in the second experiment). In the first experiment containing plas tic inorganic stimuli the fish showed a significant preference for left fin usage as a population. In the second experiment containing animal, vegetable and mineral objects there was a significant difference between laterality indices for animal and minera l and also between vegetable and mineral objects. The only significant preference found was for objects in the mineral category using the left fin to contact it (Bisazza, Lipolis, & Vallortigara, 2001). This suggests that the fin preference is dependent on what type of object the fish is investigating, and possibly which hemisphere of the brain is being used for different conditions. The European toad also displays a limb preference, but in a different kind of task (Bisazza, Cantalupo, Robins, Rogers, & Va llortigara, 1996). Bisazza et al. tested both cane toads ( Bufo marinus ) and European toads ( Bufo bufo ) for forelimb preference by
Lateralization in manatees 20 region and also using the aquatic ri ghting task, in which the toad is flipped onto its back toads did not display a preference in the paper strip test, but did display preferences in the aquatic righting task, preferring to use the right forepaw to turn over. The European toads exhibited a population level bias for the right forepaw to remove the strip of paper or balloon. These tasks, although not necessarily manipulatory, were strong enough measures to indicate a limb preference in toads. Numerous species of birds exhibit limb preferences as well, a few at the population level and a few at the individual level. In a study by Rogers and Workman (1993) chicks displayed a population level bias to use the right foot to remove a piece of tape from the beak. The researchers also tested budgerigars using the same task, and the budgerigars did not display a preference. Little owls, kestrels and buzzards display foot preferences to grasp prey in a hunting task ( Csermely, 2004). Japanese jungle crows also display a foot preference, in this case at the individual level for pulling a rubber band off the beak and for holding a bag down while they tear into it with their beak (Izawa, Kusayama, & Shigeru, 2005). Avocet s, Northern Shovellers, and Eurasian curlews do not use the feet for any sort of manipulation, but still display population level preferences for which foot they stand on while resting the other foot (Randler, 2007). Asian elephants, the closest living r elative of the Florida Manatee also display a preference not for a limb, but a side preference of trunk movements while eating grass with stronger side preferences than primate hand preferences. Martin & Niemitz (2003) recorded the trunk movements of 41 wi ld Asian elephants while the elephants fed on
Lateralization in manatees 21 and object contact (the distal part of the trunk contacting, twisting and pulling the food plant). All elephants displayed side preferences in all categories, but there was no population level bias. All elephants showed a highly significant side preference in object contact (20 favored the left, 21 favo red the right), but only 27 elephants showed a significant side preference in retrieval (17 preferred the right, 10 preferred the left) and only 24 showed a significant side preference in reaching (13 started on the right, 11 started on the left). The dist ribution of side preference combinations differed significantly from chance with more than half (22) of the preferred combinations containing the same side preference for all categories. The highest side index was for object contact. A stronger side prefer ence was correlated with faster retrieval and reaching suggesting that stronger side biases lead to more efficient performances while foraging. The authors believe that the side preference in this unpaired organ may reflect cerebral asymmetry. Object conta ct, classified as a manipulative submovement, is thought to be a more complex task with higher cognitive demands than retrieval or reaching (transport components), and this may be the reason for the stronger preference in this task (Martin & Niemitz, 2003)
Lateralization in manatees 22 Chapter 3. Marine Mammals The previously mentioned studies suggest that more complex tasks require more activity by the brain and are therefore more likely to show evidence of individual and population level asymmetries (Hopkins, 2006; Chapelain, Bec, & Blois Heulin, 2006; Vauclair, Meguerditchian, & Hopkins, 2005; Fagot & Vauclair, 1991; Martin & Niemitz, 2003). However, other, more simple behaviors also present evidence of both individual level and population level lateralization such as turning preferences in tadpoles (Wassersug, Naitoh, Yamashita, 1999), turning preferences in newts (Green, 1997) and avoidance preferences in sheep (Versace, Morgante, Pulina, & Vallortigara, 2007). Turning preferences may also imply hemispheric lateralization and are even prevalent in a few marine animals including fish (Bisazza & Vallortigara, 1997), dolphins (Sobel, Supin, & Myslobodsky, 1994), and sea lions (Wells, Irwin, & Hepper, 2006). Dolphins display a population level preference for swimming direction in a captive setting. Sobel, Supin, and Myslobodsky (1994) investigated rotational swimming in 13 Bottlenose dolphins in three differently shaped pools (rectangle, square, circle). The researchers recorded the behavior of the dolphins for the time spent circ ling clockwise, counterclockwise and random. The researchers then implemented three separate tests in an attempt to manipulate the swimming direction of the dolphins: Introduction of subject ing direction, they observed three dolphins while the spinning the water in the same and then opposite direction of swimming preference, and then tested three dolphins for ocular dominance by feeding each dolphin from either the periphery or center of the pool.
Lateralization in manatees 23 All dolphins began unidirectional circling upon entering the pool, 11 out of 13 dolphins swam in a counterclockwise direction and the circling direction was constant. Direction of circling also remained constant between pools and the position (att itude) of the dolphin when entering the pool did not affect the direction of swimming. The direction of swimming was not affected by postural priming, spinning of the water or a visual anchor in the center of the pool suggesting that the swimming direction is not determined by ocular dominance in this case. The authors suggest that the swimming imbalance may suggest the existence of intrinsic neurochemical asymmetries. California sea lions do not exhibit lateralization of swimming behavior at the populati on level, but do display individual preferences for swimming direction. Wells, Irwin and Hepper (2006) observed seven captive sea lions and recorded the direction of swimming upon entering the pool for a total of 100 episodes of swimming for each animal. A ll animals exhibited a significant bias while swimming with five of the sea lions preferring to swim in a counterclockwise direction and two preferring to swim in a clockwise direction. The lack of a bias at the population level suggests that sea lions are not lateralized at the population level for swimming behaviors; this may be due to the ease of the task or the small sample size. A beluga whale also exhibits a preference for swimming direction ( Marino & Stowe, 1997a). The researchers observed the circ ular swimming direction of a captive beluga whale, recording the direction of swimming, turning, and spinning. The whale preferred to swim in a clockwise direction in contrast to the counterclockwise direction preferred by the bottlenose dolphins. The whal e preferred to spin to the left and turn to the right, but both of these behaviors were associated with the swimming direction.
Lateralization in manatees 24 Fin whales exhibit consistent asymmetric body pigmentation with all whales having dark pigmentation on the left anterior third of the body and baleen with lighter pigmentation on the right side of the body. This pattern of pigmentation is associated with lateralization during feeding behavior. Tershy (1992) observed wild fin whales while they fed to determine their lateral lunge preference during surface feeding. The fin whales made lateral lunges most often with the right side of the body facing down. Three lunged most often with the right side do wn providing evidence that fin whales, blue level biases for feeding behavior. Humpback whales also exhibit laterality of turning during feeding behavior (discovered through jaw abrasions) as well as laterality of flipper slapping behavior at the population level, approaching the level of human handedness (Clapham, Leimkuhler, Gray, & Mattila, 2005). Clapham et al. investigated the presence of behavioral asymmetries in the humpback whale for three behavior types: breaching (whale jumps out of water head first spinning on its longitudinal axis), flippering (hitting the water with one flipper), and tail breaching (whale lifts the posterior of the body sideways out of the water). The researchers also p hotographed both sides of the jaws of whales for abrasions that occurred from feeding on the bottom. Breaching and tail breaching were not strongly lateralized, but did show a bias to the right; only flippering was strongly lateralized with a majority of w hales showing a bias for the right flipper. Out of those whales photographed that had jaw abrasions, 80 percent had abrasions on the right jaw, 20 percent showed abrasions on the left jaw and none had abrasions on both jaws. This strong population
Lateralization in manatees 25 level bi as approaches the level of handedness found in humans (90/10 split). There was a significant relationship between the side of the jaw abrasions and the flipper used during flippering and between the side of the jaw abrasions and tail breaching. These resul ts offer strong support for the presence of population level lateralization in the humpback whale in both a turning preference during feeding behavior and a limb preference during social behavior. Walruses also exhibit lateralized behaviors associated wi th anatomical asymmetries. Levermann, Galatius, Ehlme, Rysgaard and Born (2003) studied the feeding behavior of the walrus using underwater video recordings. The front flippers are used by walruses to clear away stirred sediment in front of the head while feeding on the bottom. The walruses used the right flipper more often than the left flipper to clear away sediment from the face. The researchers also measured the flipper bones of 23 walrus skeletons and compared the length of the bones in the flippers on the left and right sides of the body. The right front flipper had larger measurements than the left front flipper for the scapula, humerus, and ulna. A lifelong preference for the right flipper may strengthen that flipper more than the left through repeat ed use and could explain the link between the preference and the asymmetry. Dolphins also exhibit flipper preferences, during social flipper rubbing behaviors. Sakai, Hishii, Takeda, and Kohshima (2006) video recorded Indo pacific bottlenose dolphins duri ng the social flipper rubbing behavior in which one individual rubs another with its flipper. The researchers also recorded the eye used to inspect the researcher. The dolphins used the left flipper to rub the other dolphin in a majority of the episodes an d used the left flipper significantly more frequently than the right flipper. Out of 20
Lateralization in manatees 26 identified repeated rubbers, nine showed a significant left side bias and none showed a right side bias. Additionally, the duration of rubbings lasted significantly lon ger when the left flipper was used than when the right flipper was used. The dolphins being rubbed did not show any behavioral asymmetries. The researchers determined that laterality of this behavior resulted from interaction between the location of the ru bbee in regard to the rubbers asymmetrical behavior. The left eye was used significantly more frequently by the dolphins to inspect the researcher suggesting that the late rality of rubbing behavior may be due to a left eye preference to view the conspecific and implying a right hemisphere specialization in dolphins for interactions with conspecifics and possibly during emotional situations. Most marine mammals do not have limbs that are dexterous enough to manipulate objects, and such a task is therefore not feasible to detect lateralization. However, all marine mammals do have eyes and marine mammals do display eye preferences and differences in performance between the two eyes for certain tasks. These differences probably indicate hemispheric specialization and lateralization of the brain and have been extensively studied in the dolphin (Kilian, Von Fersen, & Gntrkn, 2000; Yaman, von Fersen, Dehnhardt, & Gntrkn, 2003 ; Kilian, Von Fersen, & Gntrkn, 2005; Sakai, Hishii, Takeda, & Kohshima, 2006; Delfour, & Marten, 2006). The right eye is dominant for visuospatial processing tasks in the bottlenose dolphin. Kilian, Von Fersen, and Gntrkn (2000) trained two adult f emale dolphins to swim through three different hoops one at a time without omitting or reusing any hoops. After the dolphins learned the task successfully, the researchers tested them in monocular
Lateralization in manatees 27 trials with one eye covered with an eyecup. Right eye perfo rmance was significantly better than left eye performance and the left eye performance differed significantly from binocular performance. The dolphins showed better monocular performance of a complex visuospatial task when using the right eye suggesting th at the right eye and left hemisphere are dominant for processing visuospatial information in the dolphin. In a different kind of visual discrimination task, dolphins also show superior performance while using the right eye (Yaman, von Fersen, Dehnhardt, & Gntrkn, 2003). The researchers tested three female dolphins monocularly in a visual discrimination task. An eyecup covered one eye while the dolphins discriminated monocularly between simultaneously presented pairs of different patterns of shapes. The researchers also recorded spontaneous eye use by the dolphins during free ranging tasks when only one eye was used. In the discrimination task the dolphins performed better when they used the right eye, and more trials were required to reach learning crit erion when the left eye was used. All three dolphins exhibited right eye superiority and a right eye preference for viewing both familiar and unfamiliar stimuli. The dolphins also acquired pattern discriminations faster when the right eye was used indicati ng left hemisphere dominance for visual object processing in dolphins, which is in accordance with the previous study. It also may indicate left hemisphere dominance for concentration on local object features. Bottlenose dolphins also exhibit right eye vi sual dominance for numerical tasks (Kilian, Von Fersen, & Gntrkn, 2005). Kilian, Von Fersen, and Gntrkn tested a male bottlenose dolphin for eye use in numerical tasks to determine whether dolphins would show a right visual field advantage for discri minating visual stimuli differing in
Lateralization in manatees 28 numerosity. The researchers tested the subject monocularly with one eye covered with an eyecup at a time. The task was to swim to the stimuli choices and choose the stimulus containing the smaller number of elements. Af ter the dolphin learned this task the researchers controlled the stimuli for equal surface area of the elements despite different numbers of elements. The dolphin displayed superior performance while using the right eye for this task with a significant dif ference between the viewing conditions. The dominant performance of the right eye for this task suggests left hemisphere specialization for numerical tasks also in dolphins. In a study investigating voluntary eye preference in dolphins, dolphins exhibit a right eye advantage when they have the choice to use either eye. Delfour and Marten (2006) tested the spontaneous eye preferences in dolphins while processing visual stimuli using a touch screen that was mounted underwater. The touch screen displayed imag es of geometrical figures and video sequences. The dolphins learned to associate different tones with certain visual images on the underwater touch screen. The computer presented shapes randomly on the touch screen while a pure tone was played to the dolph ins. The dolphin had to touch the target within five seconds of hearing the tone or the screen turned black. All three dolphins spent more time using monocular than binocular vision. Two of the dolphins preferred the left eye and the other dolphin display ed a slight preference for the right eye. In the first two test situations, one of the dolphins preferred the left eye, for the third situation, none of the dolphins displayed an eye preference. Overall, the dolphins achieved higher performance scores whil e using the right eye suggesting a left hemisphere dominance for visual stimuli in dolphins in accordance with all previous studies on visual lateralization in dolphins.
Lateralization in manatees 29 Manatees do not have laterally placed eyes like the dolphins, making eye preference i n manatees difficult to determine. Manatees do, on the other hand, posses flexible flippers similar to the walruses and may be likely to show lateralized behaviors in this regard. Both manatees and walruses feed in a similar manner using their vibrissae to detect prey in the case of the walrus, and to detect and grasp seagrasses in the case of the manatees. Both animals may also use their flippers in similar ways.
Lateralization in manatees 30 Chapter 4. Evasion Behavior and Scar Data Evasion Behavior Animals face the problem of predation by other animals daily, a problem existing for millions of years. Those most successful at evading their predators survived to reproduce and pass on their genes and therefore, their skills at evasion. Those genes passed on lateralized evasion responses in some species, even those as primitive as the trilobite of the Precambrian era (Babcock, 1993). These asymmetries of evasion behavior exist at the population level in some species (Reist, Bodaly, Fudge, Cash, & Stevens, 1987) and at the individual level in others. Lateralized eye use and hemispheric specialization for predator surveillance are the presumed causes for asymmetries of evasion behavior (Bisazza, & Vallortigara, 1997). The first evidence of a population level behavioral asym metry in fish was found in the goldbelly topminnow ( G. falcatus ) (Bisazza, Cantalupo, & Vallortigara, 1995). As the fish swam across the middle of a test tank the researchers introduced a white oval form emulating a predator. The researchers recorded the d irection of axis at the stimulus presentation and direction of turn during escape. The first experiment tested immature fish and they displayed a strong bias to escape rightwards which gradually decreased until there was a preference to escape leftwards in the fifth session. In the second experiment using adults, most of the fish exhibited a preference to escape to the right. The escape behaviors of the adults and juveniles did not differ. The researchers tested the adults in a third experiment in repeated sessions and the fish exhibited a strong bias to turn to the left in the last three sessions. Local biases of asymmetric postures of the animal at the time of stimulus presentation did not affect the lateral biases in the direction
Lateralization in manatees 31 of escape behavior as sh own by a positive correlation between data from the perpendicular and quasi perpendicular postures. Overall the fish displayed a pattern of a bias to escape to the right during initial encounters with the predator stimulus with a gradual development of a b ias to escape to the left after repeated presentations. The escape bias may shift leftwards as the fish recognizes the stimuli as harmless, when the left hemisphere of the brain takes over (Bisazza, Cantalupo, & Vallortigara, 1995). Escape behavior is la teralized at the individual level in the onesided livebearer ( Jenynsia lineata ) (Bisazza, Cantalupo, & Vallortigara, 1997). The researchers tested behavioral asymmetries in escape responses of mature males. The researchers lowered a predator shape into th e tank after the fish were habituated. They then recorded the direction of the fishes turning behavior upon seeing the predator shape. The fish were not lateralized at the population level during the first test, however the frequency distribution of rightw ard escapes differed significantly from a normally distributed population. The biases seemed to be constant, with a correlation between the turning direction in the first and second tests. Morphological asymmetries were not correlated with the degree of la terality in turning behavior. The lack of a population bias may be attributed to the solitary lifestyle of J. lineata (Bisazza, Cantalupo, & Vallortigara, 1997). The escape biases mentioned above may have arisen from preferential eye use for viewing preda tors. Goldbelly topminnows ( G. falcatus ) also exhibit a population bias for turning left and hence using the right eye to view a predator in a detour task. Facchin, Bisazza and Vallortigara (1999) tested Goldbelly topminnows separately for evasion behavior The test tank consisted of a runway in the middle with a barrier at the end of the runway containing a dummy predator. The researchers placed the fish into the
Lateralization in manatees 32 opposite end of the tank from the predator and pushed the fish along the runway with a net. Th ey recorded the direction that the fish turned when leaving the runway. Overall the fish displayed a significant bias to turn left. In a similar study using a swim way test with fish, mosquitofish ( Gambusia holbrooki ) preferred the right eye for fixating a predator (De Santi, Sovrano, Bisazza, & Vallortigara, 2001). The researchers placed female mosquitofish individually into a test tank containing a swimway with an opening at the end containing a live predator (pumpkinseed sunfish) behind glass plates. Th e fish started in the opposite side of the swimway behind a plant and the researchers recorded the eye used to fixate the predator. The fish overall preferentially used the right eye to fixate the predator and that preference became clearer as the fish app roached closer to the predator. When the fish were still a distance away from the predator, most of the fish used the left eye to view the predator and switched to the right eye as they got closer. The fish used the left eye to view mirror images of themse lves. The use of the left eye to view mirror images may indicate that the fish use the right hemisphere to monitor conspecifics, for example while schooling. The authors suggested that the right eye preference for inspecting predators indicates complementa ry specializations of the two hemispheres of the brain and that the initial use of the left eye to monitor the predator at a distance allows rapid evocation of species specific responses (escape) as the fish approached the predator to fixate it, the right eye (left hemisphere) allowed inhibition of the escape responses enabling the fish to remain and view the predator (De Santi, Sovrano, Bisazza, & Vallortigara, 2001). Three species of toads also exhibit population level evasion behavior, and the right sid e of the brain elicits the fear responses. Lippolis, Bisazza, & Vallortigara (2002)
Lateralization in manatees 33 examined escape responses in three species of anurans: the common European toad ( Bufo bufo ), the European green toad ( Bufo viridis ) and the cane toad ( Bufo marinus ). The re searchers used the rubber head of a model snake as the predator stimulus, which they presented into the testing arena rapidly on a pole using a two velocity movement. During the procedure the toad resided in the center of the arena and the stimulus came fr om the left or right side (monocular vision), or from the front (binocular vision). The researchers recorded the first behavior performed by the toad after presentation with a total of eight possible behaviors occurring. All three species had increased rea ctivity scores following stimulus presentations on the left side and in the frontal field compared to the right side. Reactivity was the weakest to stimulus presentations on their right side. B. bufo jumped forward more often when the stimulus was presente d on the left than the right. B. viridis exhibited no difference and B. marinus preferred to jump forward after stimulus presentation in the right field compared to the left. B. viridis and B. marinus exhibited a bias to jump sideways when the stimulus wa s presented on the left compared to right presentations. All three species were more responsive after left side presentations suggesting that the right hemisphere is specialized for evasion behavior compared with the left side. Specialization of the right hemisphere for controlling affective behavior such as this evasion behavior is widespread among mammals and birds (Lippolis, Bisazza, & Vallortigara, 2002). Scars as evidence Experimental studies testing for lateralization of behaviors may be successful i n determining behavioral lateralization, but other methods are available when behavioral experiments are not. The turning preferences, eye preferences and limb preferences of
Lateralization in manatees 34 animals are just a few ways to study lateralization. There is yet another way of investigating lateralization that has not been widely used but has had some success. Scar evidence can reveal lateralization of evasion behavior as well as lateralization of other behaviors (Clapham, Leimkuhler, Gray, & Mattila, 2005). Behavioral asymme tries have been found to date back at least as far as the Early Cambrian period using scar evidence. Babcock (1993) analyzed scars caused by predator attack in trilobite fossils dating from the Cambrian as well as post Cambrian trilobite fossils. A large m ajority (70%) of the specimens had injuries only on their right pleural lobe whereas only 27% of the specimens had injuries only on the left pleural lobe. The difference was significant. Anomalocaris is believed to be one of the main predators responsible for these injuries as well as arthropods, mollusks, some chordates and conodonts. These results could indicate lateralized escape behavior of the trilobites, lateralized attack behavior of the predators, or a combination of the two. Whether the lateralized injuries were caused by vertebrates or invertebrates, these results give evidence that lateralization is not a recent development, but has been manifested in animals for hundreds of millions of years. Whitefish may also exhibit population level lateraliz ation of evasion behavior based on data collected on locations and types of scars (Reist, Bodaly, Fudge, Cash, & Stevens, 1987). The researchers described scarring frequency and geographic and temporal distribution for whitefish ( Coregonus nasus and Corego nus clupeaformis ) based on specimens collected by gillnet in the Mackenzie River. In C. nasus 70% of slash scars occurred on the left side of the body differing significantly from chance. Round scars also occurred more often on the left side than the right side of the body, which was
Lateralization in manatees 35 significantly different from chance. Some of the round scars may be due to attacks of Atlantic lampreys and slash scars may be due to previous capture in gillnets and therefore laterality in evasion responses. The long slash sc ars may also have been caused by predation attempts by the northern pike, grizzly bears, and birds. The results offer physical evidence in support of population level laterality in evasion responses in whitefish. Scar evidence of lateralization also exis ts in mammals. Jarman (1972) discovered a lateral bias in the fighting behavior of male impalas. Jarman measured the complete skins from 150 individual impalas for thickness in different areas of the body. Scars found on the skin from male male fighting oc curred more often on the right forequarters than the left forequarters and more on the left hindquarters than right hindquarters. The distribution of scars differed significantly from chance suggesting lateralization of fighting behavior in the male impala It is not certain whether it is a turning preference to evade stabs, or a turning preference to stab the opponent. Lateralization as evidenced through scars was also found in marine mammals, the humpack whales mentioned in the previous section (Clapham, Leimkuhler, Gray & Mattila, 2005). The four studies mentioned above demonstrate evidence in support of using scars to investigate behavioral asymmetries in animals at the population level. By using scar data, all four studies revealed significant populati on level behavioral asymmetries in an innovative way. The Florida Manatee lives along Florida coastal waterways in constant contact with human recreation (Reep, & Bonde, 2006). In 2008, 26.7% of manatee deaths were due to watercraft (Fish and Wildlife Re search Institute, 2009). Many manatees bear
Lateralization in manatees 36 permanent scars from collision with water craft and these scars are often used to identify individual manatees due to their conspicuity (Reep, & Bonde, 2006). The presence and visibility of the scars of the Flori da Manatees makes these animals prime candidates for using scar data to infer lateralization of evasion behavior, only in this case the animals are evading boats rather than predators.
Lateralization in manatees 37 Chapter 5. Manatee Biology and Behavior The Florida Manatee ( Trichechus manatus latirostris ) is an endangered marine mammal that inhabits Florida coastal waterways. Florida manatees are strictly herbivorous and feed on over 60 species of aquatic vegetation including seagrasses growing in the sediment and pl ants like the water hyacinth that float at the top thanks to their prehensile lips. They will feed for four to eight hours a day (Reep, & Bonde, 2006). The use of the term manatee in all following cases refers to the Florida manatee. Female manatees becom e sexually mature at three years of age and males can produce sperm at two years of age, but most manatees will not successfully breed until six to ten years of age. The gestation period is 12 13 months and the calves will remain with their mothers for two to three years. Usually only one calf is produced per pregnancy, but twins have occurred rarely. The interbirth interval for manatees is two to five years although some manatees may go more than five years without giving birth (Van Meter, 1989). Manatees can live in freshwater, brackish and marine environments and are subtropical animals. In the winter, they rely on warm water sites such as natural springs and warm water discharges from power plants to stay warm. Many manatees will congregate in these are the Apollo Beach power plant and many other natural and artificial warm water sites. The population size of the Florida Manatee was surveyed and estimated to be at 3,807 manatees in Januar y, 2009 (Fish and Wildlife Research Institute). Due to the large population size and their distribution in the busy Florida waterways, manatees are often in close contact with watercraft and collisions are a major
Lateralization in manatees 38 threat to manatees. In 2008, an estimate d 26.7% of all manatee deaths were caused by collision with watercraft (Fish and Wildlife Research Institute, 2009). Increased boat registration is positively correlated with an increase in watercraft related mortality in the Florida Manatee (Wright, Acker man, Bonde, Beck, & Banowetz, 1995). Anatomy The body of the Florida Manatee is adapted to life in the water. The body is round and elongated with a flattened paddle like tail that is undulated up and down to propel the manatee through the water. Manatees have two pectoral flippers that are flexible enough to pull objects toward the body and that they also use to turn during swimming, to walk along the bottom of the water, and to dig for roots. The Florida Manatee has prehensile lips that it uses to grasp vegetation and bring the vegetation into the oral cavity using a series of rhythmic movements of the lips, bristles and jaws. There are six fields of vibrissae, or bristles, on the mouth of the manatee, four fields on the upper lip and two fields on the l ower lip (Reep, Marshall, Stoll, & Whitaker, 1998). These bristles are used in combination to bring food into the mouth and are also used in tactile exploration. The U2 bristle fields, located on the upper lip can be used prehensilely and the U2 field on t he left and right side can be used independently or together to grasp or explore objects. The U2 bristle fields are also used to pinch conspecifics during interactions and the entire snout region is swept from side to side while investigating objects (Mar shall, Huth, Edmonds, Halin, & Reep, 1998). These hairs on the face of the manatee are classified as sinus hairs based on the microanatomy of the follicles, which contain a true ring sinus (Reep, Stoll, Marshall, Homer, & Samuelson. 2001). The postcranial hairs, however, are not classified as sinus
Lateralization in manatees 39 hairs but do meet the criteria to classify as tactile hairs, as they lack a true ring sinus but do possess a follicle sinus complex. These hairs might be used like the lateral line of the fish to detect water di splacements and approaching conspecifics (Reep, Marshall, & Stoll, 2002). Information about the neuroanatomy and brain of the Florida manatee is reviewed in Appendix D. Manatee Boat Avoidance Boats often hit manatees, but it is not due to a lack of manate es trying to get out of the way. Manatees use two main strategies by which to avoid boats, by diving and by swimming to deeper areas. Manatees may attempt to escape boat strikes by diving as suggested by scar patterns (Wright, Ackerman, Bonde, Beck, & Ban owetz, 1995). The researchers examined two groups of watercraft related deaths in the manatee, propeller and impact. The researchers measured the wound components and compared scars and fatal wounds from propellers. Impact deaths were fatal strikes from th e hull, rudder, keel or other blunt scars on sketches and photographs and divided the carcass into regions consisting of head, dorsal thorax, dorsal mid body, dorsal a bdomen and tail. Only 2% of all the scars found on the carcasses occurred on the head, 43% occurred between the head and the center of the back, and 55% occurred behind the center of the back to the end of the tail. These proportions suggest that the manat ees may have been attempting to escape by diving when they were hit. Only 11% of the scars were perpendicular to the head tail axis suggesting that in 89% of the strikes the manatee was directly facing or moving directly away from the boat at the time of i mpact.
Lateralization in manatees 40 In a behavioral study the manatees responded to approaching boats at distances of 20 25 meters away from the manatee primarily by moving toward/into deeper water and increasing swimming speed (Nowacek, Wells, Owen, Speakman, Flamm, & Nowacek, 2004) Researchers observed individual manatees during both opportunistic and experimental vessel approaches. Opportunistic approaches occurred when a vessel operated by an unaffiliated individual approached or passed a focal manatee and experimental vessel app roaches were conducted by the researcher passing the boat greater than three body lengths away from the subject. The researchers used a camera attached to a blimp to record the behavior of the manatee during the boat passes and during control periods. Beha was also recorded. During 170 passes with 30 manatees, 49% of the passes were associated with at least one behav ioral change. There were significantly more changes in behavior during vessel approaches than during control segments. These behaviors included turning toward deeper water and increases in swimming speed. In 37.5% of the passes the manatees turned toward or into channels as the boat approached. The swimming speed changed in 19.7% of the boat passes, and 90% of these changes were increases in speed. The responses were significantly affected by approach distance and both boat and manatee habitat (Nowacek et al., 2004). It appears that manatees also exhibit responses to approaching boats and these responses seem to represent attempts to escape a collision by diving into deeper water or swimming faster.
Lateralization in manatees 41 Although these studies indicate that manatees prefer to dive to avoid boats and swim to deeper water, neither study examined the lateralization of scars on the body or lateralization of escape behaviors. When boats are going at high speeds, manatees may not have enough time to determine where the boat is coming from before they are struck. It is possible that the manatees dive to one side or another to avoid boats at the last minute, and this avoidance response may be mediated by one specialized hemisphere of the brain as it has been in other species. All of th e studies mentioned earlier provide strong support of the theory that lateralization of the brain manifests itself in limb preferences. The mere fact that both population level and individual biases have been found in animals as diverse as fish, elephants and chimpanzees is testament to its importance in the animal kingdom. The correlation of results between studies supports behavioral asymmetries as a tool to indicate cerebral lateralization in animals, such as the studies using eye preference to determine hemispheric specialization. As lateralization has been found in so many species for so many tasks, it makes sense to use behavioral preferences to infer hemispheric lateralization. Lateralization has not been studied in the Florida manatee, and as the Fl orida manatee is a protected species it would be beneficial to procure information about how the brain of the manatee is organized using a non invasive observational method such as limb preference, to determine if they also show lateralized brain functions Previous elephant (Martin & Niemitz, 2003), another marine mammal, the dolphin (Sobel, Supin, and Myslobodsky, 1994), as well as limb and eye preferences in other marine animals,
Lateralization in manatees 42 such as fish (Bisazza, Rogers, &Vallortigara, 1998). The conspicuous scars, which reside on the backs of many manatees, make it desirable to use these scars to infer lateralization of evasion behavior in the manatee. Manatees often use thei r limbs to move objects, to swim and to walk along the substrate. This dexterity of the limb might lead to preferences for certain behaviors. I examined flipper uses in manatees for evidence of behavioral lateralization at the population and individual le vel. Based on the intermediate status of the sociality of the Florida manatee as a semisocial species, a population level bias is not expected, but something close to a population level bias. I also investigated the uniformity of preferences across tasks a nd consistency of preferences over time. I expected that manatees would display different preferences for different tasks based on past literature finding such differences in apes. Finally, scar patterns from boat strikes were examined for evidence of late ralization of evasion behavior. Manatees do not have predators and as they are also not strictly social, are not expected to show lateralization of avoidance responses. Both wild and captive animals were used in the study to determine whether manatees hav e lateralized behaviors, and to infer possible hemispheric specializations in the manatee. Method Permits A Special Use Permit was obtained from the Fish and Wildlife Service and the Crystal River National Wildlife Refuge allowing the researchers to obs erve the manatees underwater from January 1, 2008 through March 31, 2008 in the Crystal River area.
Lateralization in manatees 43 Subjects Observations were made near the Three Sisters Springs sanctuary area of Crystal River in Crystal River, Florida. The observation period lasted fro m January 6 through January 28, 2008. 123 different wild manatees were observed during this time. In addition, 16 captive manatees were observed for comparisons between captive and wild populations. These manatees were housed in four different locations: L owry Park Zoo in Tampa, Florida; Parker Manatee Aquarium in Bradenton, Florida; The Living Seas at Epcot in Orlando, Fl; and Mote Marine Aquarium in Sarasota, Florida. Data for ten of the captive manatees was obtained from Kate M. Chapman (unpublished data ). Ages and genders were not known for all wild manatees, however this information was available for the captive manatees. Eleven male and five female manatees were observed in captivity ranging from juveniles to adults. Thirteen of the captive manatees w ere manatees that had been injured or orphaned and were brought into captivity for temporary rehabilitation to be released at a later date. Materials Wild observations: The two researchers used an inflatable two person Sevylor kayak to travel to the obser vation location each day. A kayak was used to reduce anthropogenic noise and disturbance in the river. Each researcher had a small, eight inch dive board on which they recorded their observations using dive pencils. Each researcher also had a Fuji Film wat erproof camera to take pictures of the notable scars or physical characteristics of the manatees that they observed.
Lateralization in manatees 44 Captive Observations: The observers watched the manatees from outside of the glass observation areas of the tanks at each location. Observ ations were written on a coding sheet. Procedure and Coding Wild observations: Each manatee was observed for 10 30 minutes or until it swam too far for the researchers to follow. Actions were only recorded if the researcher d both pectoral flippers simultaneously. Each researcher first wrote or drew a description of the notable physical characteristics of the manatee that was being observed (scars, barnacles, algae etc) and, if possible, the gender and general age of the mana tee (calf, juvenile, adult). Due to the small size of the dive boards and the difficulty of writing and observing at the same time, shortened codes were used to some cases, by a number. See Appendix A for the list of codes and the definitions. The actions observed in the wild consisted of locomotion, substrate touches, body touches, digging in the substrate, touching other manatees, grabbing of ropes, tourists, and bo ats. In captivity other behaviors were observed in addition to those observed in wild manatees: feeding, pulling out of the water, and playing with enrichment devices. Actions were tallied frequencies rather than bouts and a number following the code for the action recorded the number of times that an action occurred. For example, RL7 denotes that the manatee used the right flipper to locomote through the water seven cons isted of one entire circle of the flipper. Other actions were recorded separately if an interval of a few seconds occurred between the actions, or if a new action began.
Lateralization in manatees 45 At the completion of the day, each researcher entered her observations into an Excel file on the computer, double checking to make sure the correct codes were transcribed. Researchers later compared their identifying characteristics to determine if both had observed the same manatee. All manatees were assigned a title consisting of the le tter M followed by a two digit number for one researcher, and for the other researcher the manatees were assigned a title consisting of the letter M followed by a number and a letter, unless the same manatee was observed by both researchers in which case i t was given the two digit number. In a few cases manatees were observed more than once on different days. In these cases, the observations from all days were combined for the total observations for that manatee. Captive Observations: The same information was recorded for captive manatees, as was recorded for the wild manatees. During captive observations, the researcher used a clipboard and data sheets. See Appendix B for an example of the data sheet. The actions, flipper used, number of flipper uses and i n some cases, object, were recorded. Each manatee was observed for at least 30 minutes or until more than 100 unimanual flipper uses were recorded. Reliability Four of the captive manatees originally observed by Kate M. Chapman were observed at a later da te by Kara Tyler to test for the consistency of preferences across time, and also to test for reliability of the preference scores across time and observers. Three manatees were observed four years later and by a different observer on each occasion, and on e manatee was observed one month later by the same observer. All four
Lateralization in manatees 46 manatees displayed the same side preference during the second observation period with a correlation between the overall handedness scores of r (3)=0.846. Scars For each of the wild mana tees that the researchers observed, a description was written or drawn often using scar descriptions to identify individual manatees. Even if only three or four flipper uses were observed, the researchers still wrote a description for every manatee. This m ade it possible to use these scar descriptions to analyze lateralization of evasion behavior. The side bias of scars was determined using the scar side bias of each individual manatee that had one or more scars. An average was taken of these scars to dete rmine the scar side bias for that individual manatee. For example, if a manatee had a scar on the right and a scar in the middle it was counted as one right bias, or if a manatee had one left scar and one right scar it was counted as one middle bias. Only those scars that were clearly caused by watercraft collision were used. A scar was considered clearly the result of collision with watercraft if it consisted of a row of equally sized and equally spaced horizontal (or vertical, depending on the angle) scar s that are caused by propeller strikes. The other type of scars used were long, usually shallow, narrow single lines caused by the hull, keel or rudder of a boat (Wright, Ackerman, Bonde, Beck, & Banowetz, 1995). The side bias of each individual was reco rded and the numbers of scar biases of each side (left, right, midline) were added together. A total of 46 scar biases from the wild manatees were used in the analysis. Data Analysis
Lateralization in manatees 47 For each manatee a Handedness Index (HI) score was calculated using the same formula developed by Hopkins et al. (2005) by subtracting the number of left limb responses from the number of right limb responses and dividing that number by the total unimanual responses. HI scores ranged from 1.0 to 1.0, negative scores represent a left limb bias and positive scores represent a right limb bias. The absolute value of the score represents the strength of the preference. Absolute values have the following strengths: 0 0.09 represents no bias; 0.1 0.49 represents a weak bias; 0.5 1.0 represents a strong bias. An overall HI score was calculated for each manatee along with a separate HI score for each activity. Additionally, Binomial Z scores were calculated for each manatee for each activity. For the scar data, a Chi Square Goodness of Fit test was used to determine if the distribution of scars differed significantly from chance. All tests used an alpha level of 0.05. Results Out of the 123 wild manatees observed, only 25 manatees were observed for a long enough period to be included in the analysis of overall preference. A minimum of 50 overall unimanual flipper uses had to be observed for an individual manatee to be included in the overall category. The overall category combined the flipper uses for all behaviors to calculate a HI scor e that took all behaviors into account. For each separate behavior, a manatee could be included in the analysis if a minimum of 20 unimanual uses were recorded for that single behavior. All 16 captive manatees were included and more than 100 unimanual use s were observed for each captive manatee. The same criteria were used to determine whether a captive manatee was included in each separate behavior analysis, a minimum of 20 unimanual uses for that behavior alone.
Lateralization in manatees 48 The minimum number of 20 was chosen base d on a correlation. The absolute values of the HI scores were correlated with the total number of unimanual uses. A correlation with all scores for all manatees displayed a significant negative correlation between the number of unimanual uses and HI scores r (104)= 0.24404, p =0.0121 indicating that a smaller number of observations caused higher HI scores merely due to sample size effect. A second correlation revealed that this effect was not present if only manatees with 20 or more uses were included, r (67) = 0.07594, p =0.5382. Individual Preferences The numbers of manatees displaying left, right, or no preference for each behavior are shown in Figure 1. The only three categories shown are left, right and none. The preferences were not divided by strength a s very few manatees displayed strong preferences, and none of the overall preferences were strong. The wild and captive manatees were then divided as both populations exhibited different behaviors more often. The preferences of the wild manatees can be see n in Figure 2, and the preferences of the captive manatees can be seen in Figure 3. The captive manatees displayed more feeding behavior and more substrate walking than the wild manatees, along with more self touching and other touching behavior. The wild manatees displayed more flipper uses during locomotion behavior and also displayed more digging behavior than the captive manatees, although only a few manatees were seen displaying this behavior and only a few instances were seen for each manatee that was seen digging. An ANOVA ( F( 40)=0.8085, p =0.3741) revealed that the wild and captive manatee populations did not display significantly different overall preferences. The differences between the two populations for the substrate behavior also revealed that the
Lateralization in manatees 49 populations did not differ significantly F (37)=3.2642, p =0.1794 so the populations were combined for the remaining analyses. Although the populations did not differ significantly, this may be due to the smaller size of the captive sample for both meas ures. The data from smaller sample sizes are not as reliable and stable as those from larger sample sizes. There might be a difference between the two populations if a larger sample size were used. Population Preferences The population distribution of fl ipper preferences was calculated using the Chi squared goodness of fit test for the overall handedness index score and also separately for each behavior, as the behaviors appear to reveal different preferences for the manatees. The values for each of the C hi squared goodness of fit tests can be seen in Table 1. The overall preferences did not differ significantly from a distribution expected by chance ( 2 (2, N=41) = 5.32 p =0.07, =0.25 ) suggesting an ambipreferent population. However, the probability value of less than 0.10 suggests that the population displays a tendency towards the left (Fagot & Vauclair, 1991) with more manatees displaying a preference for the left flipper overall. The distributions of the preferences for the separate behaviors also did n ot differ significantly from chance. As a population, manatees displayed a tendency to prefer the left flipper overall, and slight tendencies towards the left during locomotion and during feeding. Task Differences The distribution of preferences is diffe rent for the different behaviors. More manatees prefer the right flipper for substrate touches, more manatees prefer the left
Lateralization in manatees 50 flipper for feeding and more wild manatees prefer the left flipper for locomotion. These different preferences may not be inconsis tent and may be the result of multi tasking. A preference for one flipper while walking along the bottom may leave room for the other flipper to specialize in other tasks. These differences can be seen visually by looking at figures 1, 2, and 3. Appendix C displays the handedness index scores for each manatee for each activity, for all manatees with 50 or more unimanual uses only. Manatees with fewer than 20 unimanual uses were not included in the analyses of behavior preference. It is interesting to note, however, that although only twelve wild manatees were seen eating and only a couple of uses were seen for each of those manatees, eight out of the twelve used the left flipper only, or more often than the right flipper. Scar evidence The distribution of s car biases found on the wild manatees observed differed significantly from a chance distribution, 2 (2, N=46)=9.9565, p =0.0069, =0.33. Twenty five scar biases were for the left side of the body, 13 were for the right side of the body and 8 were for the mi Binomial Tests For each manatee and for each behavior a Binomial Z score was calculated for each manatee that was included in the Handedness Index analyses. Significant negative or positive Z scores denoted left or right prefe rences, respectively. Z scores that were not significant were classified as not displaying a preference. Table 3 presents the total number of manatees classified as having a left preference, a right preference, or no preference for each behavior as determi ned by Z score significance. Although more manatees were categorized as being ambipreferent due to the very conservative nature of
Lateralization in manatees 51 the Z score analysis, the relative proportion of left and right preferences using the Z scores are very similar to those foun d using the Handedness Index scores. Both the Z scores and HI scores indicated more left preferent manatees than right preferent for the overall scores, more right preferent manatees for substrate touch, an equal number of right and left preferent manatees for locomotion, and more left preferent manatees for feeding. Discussion The population results support the hypothesis that the manatees, as an intermediate social species, show a tendency towards a left flipper preference at the population level. This theory model of lateralization, with more social species expected to display stronger population level preferences. The tendency displayed by the manatees does not qualify, however as a significant population le vel bias. A population level tendency is determined by a probability value of less than 0.10 and a significant population level bias is determined by a probability value of less than 0.05 according to Fagot & Vauclair (1991). The manatees resemble their re latives, the elephants, in not exhibiting a significant population level bias (Martin & Niemitz, 2003). However, unlike the elephants the manatees do not all exhibit preferences as some individuals were classified as ambidextrous and very few individuals s howed strong preferences. Although the Z scores revealed many more ambipreferent manatees than left or right preferent, this is likely due to the number of observations for each manatee and the very conservative analysis. The Handedness Index seems to be a much more sensitive test
Lateralization in manatees 52 to detect weak preferences and should be used in cases of animals not expected to show strong preferences. Despite these findings, the Z scores still showed similar proportions of left and right preferent manatees as the Handedne ss Index scores. The separate behaviors did not demonstrate population level preferences, but this is more likely due to the small sample sizes for these behaviors and the small number of observations for these individual manatees. A sample size of 20 obs ervations might even that for the feeding behavior the wild manatees showed a bias (not analyzed) towards the left flipper (eight out of twelve manatees) and for gra bbing behavior the wild manatees displayed a bias towards the right flipper (six out of seven manatees). These tendencies, although not officially analyzed, are consistent with the tendencies that were analyzed in captive manatees suggesting consistencies in preferences for these behaviors between the two populations. These preferences were based on only a couple of uses for each manatee and could not be included in the analyses. Both grabbing and feeding seem to be more complex or higher level behaviors (Fagot & Vauclair, 1991) than the other behaviors require more fine manipulation than locomotion, substrate touches, and manatee touches. The small number of observations might be enough to detect a bias in the more complex tasks such as these and these few observations suggest that more observations of these behaviors in future studies might reveal population level biases. Consistency
Lateralization in manatees 53 Despite the weak preference classifi cation (none of the manatees exhibited a strong overall preference), these preferences do appear to be consistent over time, based on four subjects studied for reliability. This indicates that manatees do appear to possess consistent individual level biase s, whereas a population level bias is not clear. I did not expect manatees to display strong individual preferences as strong preferences are more likely to occur for more difficult, manipulatory activites (Martin & Niemitz, 2003) and the activities that t he manatees were observed performing most often were seemingly simple non manipulatory activities such as locomotion and substrate walking. Task complexity The manatees displayed different preferences for different behaviors, supporting the theory of task complexity (Fagot & Vauclair, 1991; Hopkins, 2006; Chapelain, Bec, & Blois Heulin, 2006; Vauclair, Meguerditchian, & Hopkins, 2005). These results are contrary to the results obtained for the elephants (Martin & Niemitz, 2003) in which individuals display ed the same side preferences across all three behaviors that they performed. In this case, many manatees displayed different preferences for different behaviors (See Appendix C). Different directions of preferences are also evident in Figures 1, 2, and 3. The different preferences for different behaviors may be the result of multitasking (Vallortigara, Rogers, & Bisazza, 1999) If one flipper is preferred or specialized for certain tasks, the other flipper is free to perform other behaviors at the same tim e. A manatee could use one flipper to walk along the substrate or swim while the other is used to bring food to the mouth. While the captive manatees were eating one flipper would hold the food to the mouth while the other would be used to swim through th e water or to
Lateralization in manatees 54 may use different flipper preferences to enhance their ability to multitask. Evasion behavior shows a population level bias in manatees, and this could be seen as a complex or high level task. When manatees are forced to evade a speeding boat, they may rely on a cognitively complex fear response that controls their behavior to evade. The fact that this behavior shows a population level bias and seemingly req uires more cognitive energy supports the theory that more complex or high level tasks are more likely to reveal population level lateralization (Fagot & Vauclair, 1991). Environment differences The environment that the manatees lived in at the time of the observations did not affect their flipper preferences, although different behaviors were observed in different proportions in the two environments. One of the captive manatees, Snooty, lived his entire life in captivity in close contact with humans. He al so displayed a constant right flipper bias over four years. What is more interesting is that three of the five manatees (calves and juveniles) that were observed while living with him also displayed a preference for the right flipper and the other two were ambipreferent. Whether the preferences of these manatees were influenced by their experience with an older right handed manatee or by the flow of water in the aquarium is unknown but both should be looked into as possible factors in future studies. Althou gh water flow of the tanks was not recorded, previous studies of captive dolphin swimming preferences suggest that water current in the tank does not effect swimming direction preference (Ridgway, 1972; Marino & Stowe, 1997b; Sobel, Supin, Ya & Myslobodsky 1994) and it would not be expected to affect flipper preferences in manatees. Hugh and Buffet, who have lived
Lateralization in manatees 55 together in the same tank for many years and are also half brothers, both display consistent left flipper preferences. Again in this case, they may have similar preferences due to shared genes or due to the mechanics of the aquarium in which they live. Evasion behavior The significant bias of scars on the left side in the sample of manatees observed may indicate lateralized evasion behavior in th e Florida manatee. The manatees might have a bias of swimming to their right when they see or hear a boat that is approaching very quickly and/or very close. If this behavior occurs at the last minute, they may not completely avoid the boat and as they are swimming to the right the left side is hit. This information is not enough to discern whether it is a factor. Observations of other species suggest that it would not be a factor in the turning preference. The goldbelly topminnow, at the time of evasion (Bisazza, Cantalupo, & Vallortigara, 1995). This right avoidance in the man atees is similar to the population level bias in sheep to avoid obstacles to the right ( Versace, Morgante, Pulina, & Vallortigara, 2007). If the manatees are turning right when the boat approaches this suggests that they are using the right flipper and pos sible control by the left hemisphere of the brain. The behavioral observations of locomotion preferences indicated a bias to prefer the left flipper under normal circumstances, and therefore control by the right hemisphere. Perhaps the right hemisphere is used by manatees during leisure time and normal activity, and the left hemisphere becomes active during fear causing the manatees to use the right flipper and turn to the right. Observations of manatees in both captivity and the wild indicate that
Lateralization in manatees 56 manatees use the right flipper to turn to the right and the left flipper to turn to the left. In toads, the right side of the brain elicits the fear response (Lippolis, Bisazza, & Vallortigara, 2002) and the left side of the brain may control the fear response in Goldbelly topminnows (Facchin, Bisazza, & Vallortigara, 1999). Behavioral observations should be conducted to determine if the left hemisphere might elicit the fear response in manatees as well. Manatees currently do not have any natural predators besides a few rare instances of large sharks (Reep & Bonde, 2006). If this population level evasion response is a true phenomenon, the question is why the manatees display this bias. According to e caused by differences in success of certain biases and predation pressure. Predation pressures have not caused this behavior to become lateralized at the population level, unless this bias is left over from previous relatives of the manatee during the ev olutionary history or from unknown predecessors to the manatees might have been lateralized at the population level and may have experienced predation pressures. Ce rtain weaknesses of the current study should be addressed in future studies by observing more manatees for longer periods of time and focusing on more manipulatory behaviors such as grabbing, digging and feeding. The different preferences across behaviors suggest that the preferences should be looked at separately by behavior. Although the results suggest that manatees do not display a strong population level bias, only a tendency, future studies using more observations for each manatee may find a populatio n level bias. The current results do suggest consistent individual level bias and
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Lateralization in manatees 66 Yaman, S., von Fersen, L., Dehnhardt, G. & Gntrkn, O. (2003). Visual lateralization in the bottlenose dolphin ( Tursiops truncatus ): evidence for a population asymmetry? Behavioural Brain Research, 142 109 114. Table 1 Chi Squared values for each behavior. Task Chi Squared DF N p Overall 5.3171 2 41 0.0701 Substrate 4 .2041 2 49 0.1222 Locomotion 1.4000 2 30 0.4966 Feeding 4.5455 2 11 0.1030 Self touch N/A N/A 3 N/A Other touch N/A N/A 7 N/A Grab N/A N/A 2 N/A Dig N/A N/A 1 N/A The cells containing N/A are tests that could not be run due to inadequate sam ple sizes, or expected frequencies of less than 5.
Lateralization in manatees 67 Table 2 Preferences over time Subject Day Age HI Substrate Feeding Swimming Self touch Other touch Grab Hugh 1 A 0.2457 1 0.1818 0.2812 0 Buffet 1 A 0.1373 0.25 1 0 1 Sister 1 Y 0.4261 0 1 0.6338 1 Snooty 1 A 0.4247 0.375 0.5 0.2308 Hugh 2 A 0.1393 0.0978 0.2068 0.085 0.5 Buffett 2 A 0.38 0.2101 0.68 0.3714 0.3684 Sister 2 Y 0.4268 0.4419 0.4333 Snooty 2 A 0.11 73 0.2407 0.125 0.7143 0.4118 0.5294 *Day 1 indicates the first day that the measure was taken, day 2 indicates the follow up observations, 4 years or 1 month later.
Lateralization in manatees 68 Table 3 Number of manatees displaying each preference using Z scores. Task Left Right Ambipreferent Overall 12 9 20 Substrate touch 5 12 32 Locomotion 6 6 18 Feeding 5 1 5 Grabbing 0 1 1 Digging 1 0 0 Self touch 0 0 3 Other touch 1 0 6
Lateralization in manatees 69 Figure 1 Number of manatee s displaying each flipper preference across the different behaviors, for all manatees.
Lateralization in manatees 70 Figure 2 Number of individual wild manatees displaying each preference across behaviors.
Lateralization in manatees 71 Figure 3 Number of capti ve manatees displaying each preference across tasks.
Lateralization in manatees 72 Appendix A Coding Scheme and definitions. To make it easy to write down fin movements while in the water and to miss as little as possible while doing it we devised a shorthan d coding scheme for this specific project. The code consists of 2 letters followed in some cases by a number. The first letter is the fin used: R= right L= left B= both The second letter stands for the action: S touching, pushing off or pulling the body around the substrate (sand in this case, sometimes rocks) L locomotion, 1 locomotion is 1 case of the fin making a full circle back to where it started in order to move the manatee through the water, touching only the water. O other, O was written in ca ses where the manatee touched another manatee. B body, a body touch occurs when the manatee touches its own body, or holds the fin manatee would be rolled over for be lly rubs, it would touch one of the fins to the body. M mouth, in the case that we were able to discriminate which side of the mouth the manatee was using to grasp food or chew. G grab, when the manatee used a fin to grab a person, boat anchor or other s tanding objects in the water F feeding, when the manatee was clearly using his or her fin to push food further into the mouth. D digging this is observed in manatees digging holes into the substrate in search of roots, the mouth is often used in conjun ction with the fins for digging. The number following the two letters indicates the number of times that specific fin performed that specific action before being interrupted by either a few seconds time or another action, for example RL6 denotes that the right fin was moved 6 full circles in a Locomotory action before being interrupted by a different action or a few seconds time.
Lateralization in manatees 73 Appendix B Example Coding Sheet Observer: Date : Focal animal: Location: Sex: Age: Time Observed: Flipper Used Action Number of uses Object Notes
Lateralization in manatees 74 Appendix C Handedness scores Subje ct Enviro nment HI Substr ate Feedin g Swim ming Self touch Other touch Grab Dig M03 W 0.273 0.259 1 . M25 W 0.111 0.024 0.583 33 . M16 W 0.06 0.041 7 0.5 1 M17 W 0.346 0.444 0 1 M28 W 0.420 2 0.428 0.4 0.375 . M42 W 0.111 0.636 1 0 1 1 0.4 M57 W 0.14 0.111 0.176 . M51 W 0.187 0.016 7 1 0.2 0.5 0.913 M59 W 0.229 0.875 0.186 1 M26 W 0.108 0.016 0.538 1 M27 W 0.108 1 0.2 1 M31 W 0.238 0.196 0.467 0.5 M32 W 0.235 0.243 0 1 1 1 M38 W 0.1 0.104 1 1 1 M47 W 0.053 0.172 1 0.12 1 1 M52 W 0.143 0.143 0.185 1 1 M55 W 0.258 0.227 0.299 1 1 M63 W 0.016 0.263 0. 081 0.143
Lateralization in manatees 75 M64 W 0.478 0.754 0.214 0 M70 W 0.187 0.25 0.235 1 0.778 0 M0A W 0 0.142 85714 3 0.6 . M21 W 0.2 1 0.5 0.230 76923 1 . M1W W 0.14 0.142 85714 3 1 0.111 11111 1 1 1 1 M2D W 0.04 1 0.056 60377 4 1 M67 W 0.389 0.391 0.621 0.111 Jack. C 0.277 0.278 0.286 1 0.143 Baron C 0.233 0 0.353 0.667 0.4 Beac h Boy C 0.133 0.169 1 0.176 Hurri cane C 0.134 0.44 0.627 1 0.027 Gene C 0.109 0.158 0.243 0.143 Hurr. Bay C 0.309 0.333 0.231 0.333 Hugh C 0.139 3 0.097 8 0.206 8 0.281 2 0.085 0.5 Buffe tt C 0.38 0.210 1 0.68 0 0.371 4 0.368 4 Snoot y C 0.117 3 0.240 7 0.125 0.633 8 0.714 3 0.411 8 0.529 4 Whita ker C 0.038 2 0.113 9 0.015 9 0.091 0.04 0.333 Bock C 0.06 0.187 5 0.544 5 0.087 8 1 0.6 Lou C 0.306 6 0.812 5 1 0.3 0 1 Sister C 0.426 8 0.441 9 1 0.433 3 .
Lateralization in manatees 76 Coral C 0.128 2 0.111 0.127 7 0.2 Corall ee C 0.032 3 0.692 3 1 0.378 2 0.428 6 LilNa p C 0. 098 9 0.29 0.076 9 0.125 0.333 Appendix D Neuroanatomy of the Florida Manatee Brain anatomy The brain of the Florida Manatee can not be studied very invasively to a large extent due to the protected status of these animals, however some information is known quite small, and the olfactory system has been reduced while the isocortex has increased in size and probably importance. Additionally, researchers have mapp ed out certain areas of the cerebral cortex. The Florida manatee has a brain that exhibits a highly lissencephalic condition lissencephalic condition (absence of convo lutions on the cortical surface) has been typical of the sirenians throughout their evolutionary history. The cortical surface is generally lissencephalic. The brain has a deep and vertically oriented lateral fissure as well as a fissure emanating caudally from the dorsal margin of the lateral fissure. The boundaries between major brain regions are well defined and the lateral ventricles are large. The volume of the brain represented by the telencephalon is 71% and 90% of this brain region is represented by cerebral cortex. This telencephalic volume is comparable to that of primates. There are no consistent left right differences for estimated cortical volumes. The gyration index is averaged at 1.06, also with no left right differences. The
Lateralization in manatees 77 brain volumes fou nd are comparable to those of dugongs. The authors suggest that the thick underlying white matter of the brain may constrain the gray matter preventing the development of convolutions and contributing to the highly lissencephalic condition of the brain. Sirenians were also found to have low encephalization quotients, which are The mean encephalization quotient is 0.275. The encephalization quotient found for dugongs 0.189. The relative size of the sirenian brain is much lower than that predicted by allometric relationships derived for other marine mammals. The reasons for this could be expla ined by the life history traits of the sirenia. The life history trains of the sirenia are associated with larger brained species: a low metabolic rate, close to one year gestation period, sexual maturity at 5 10 years, a litter size of one, an interbirth interval of 2 5 years and a life expectancy of 50 60 years. Manatees are consumers of tropical seagrass, which has a low nutrient content. Therefore, the authors suggest that the small encephalization quotient may be due to selection for large body size in the sirenia without an effect on brain size. There is no evidence supporting a continued relationship between increasing brain size and increasing body size during postnatal growth. There is a curvilinear relationship between brain mass and body length in Florida manatees suggesting that most of the postnatal growth in brain size occurs before weaning. These results suggest that sirenian evolution has selected for prolonged postnatal growth phases least subject to pleiotropic effects, which resulted in gre ater body size without increasing
Lateralization in manatees 78 the brain size. The low metabolic rate and prolonged postnatal growth can account for the low encephalization quotients. Manatees along with other marine mammals, including pinnipeds have reduced olfactory systems, schizo cortex and hippocampus but have relatively large isocortices. Reep, Finlay, and Darlington (2007) estimated the volumes of 29 brains representing five orders of mammals. The external and internal olfactory systems are greatly reduced in the marine mammals. The researchers found also that the isocortex increases the most rapidly with respect to brain size and that the size of any brain structure is closely related to the overall brain size. The marine mammals have noticeably reduced paleocortex, schizocortex and hippocampus whereas the septum and amygdala are unchanged. suggest that there is not an obligatory relationship between limbic system and isocortex. They also sugges t that the reduced olfactory bulb in marine mammals is due to the decline of an unused sensory system and the reduction of the olfactory and schizocortex might be caused by the denervation from the reduction of the olfactory lobe. The changes in structure sizes and relations are possibly due to evolutionary selection for different structures or functions at the cost or size of the less used structures or functions. Researchers have mapped out the cerebral cortex of the manatee and regions were identified f or the frontal region, caudal region and for the somatosensory cortex. Areas of the thalamus, brainstem and facial motor nucleus have also been analyzed. The frontal region of the manatee cerebral cortex contains 13 distinct regions based on laminar organi zation and the cortical areas are organized into concentric zones of allocortex, mesocortex and isocortex (Reep, Johnson, Switzer, & Welker, 1989). The researchers
Lateralization in manatees 79 believe that the frontal polar cortex (area FR) and the dorsolateral cortex (area DL) serve as the prefrontal cortex with areas DL2, cluster cortex two (CL2), and the dorsal cortex (area DD) as possibilities for serving somatic sensorimotor functions. The cell clusters found in the CL areas share staining properties of the barrels found in rodent s and may perform similar functions. Area CL1 contained larger clusters, which may correspond, to the tactile bristles of the upper lips and CL2 may correspond to the shorter bristles of the lower buccal pad. In addition to these frontal areas of the cere bral cortex, researchers identified 11 new cortical areas in the caudal region of the manatee cerebral cortex (Marshall, & Reep, 1995). These new areas made a total of 11 new cortical areas in the caudal region and a total of 29 cortical areas in the brain with 24 areas described in detail and five with only the location known. The functions of these areas are not known for sure, but the researchers assigned functions to each area and based their suggestions for the functions on the cytoarchitecture of eac h area. In addition to the lissencephalic condition of the manatee brain, a few other peculiarities exist. Certain structures in the manatee brain are specialized for somatosensory functions and somatosensory structures are well represented in the brain o f the manatee which all support the manatee as being a somatosensory specialist using the facial and postcranial hairs to explore the world. The somatosensory cortex (SI) occupies about 25% of the total cortical area supporting manatees as being somatosen sory specialists (Sarko, & Reep, 2007). One third of the total cortical area is devoted to primary sensory areas, with over 50% of the frontal cortex being devoted to primary somatosensory cortex in adults and juveniles. Primary
Lateralization in manatees 80 auditory and visual areas c ombined take up 12% of the caudal hemisphere. Primary somatosensory areas of the cortex include areas dorsomedial cortex area 3 (DM3) and 2 (DM2), dorsolateral cortex area 1 (DL1) and 2 (DL2), cluster cortex area 1 (CL1) and 2 (CL2), and portions of the do rsal cortex (DD). Area DM3 probably encompasses the tail representation of the somatosensory cortex due to its dorsomedial location. Area DL1 is a likely candidate for the body representation in the somatosensory cortex. Area CL2 is the best possibility fo r the representation of the body in the medial portion and the flipper and face in the lateral portion. Area CL1 is likely to represent the face due to cytochrome oxidase staining of the largest Rindenkerne present in the cortex. The large extent of the to tal cortical area occupied by SI (25%) supports manatees as being somatosensory specialists. The Florida manatee also possesses disproportionately large principal somatosensory regions in the brainstem and thalamus relative to nuclei for other sensory mo dalities (Sarko, Johnson, Switzer, Welker, & Reep, 2007). Disproportionately large components of the auditory system are visible in the brainstem: the inferior colliculus and developed disproportionately large and presumably represents the fluke; the larger siz e might be to represent the vibrissae found on the fluke. The trigeminal components in the manatee, particularly the principal sensory nucleus, are much larger and more elaborate than in other species. The large size but lack of barreloids of the ventropos terior nucleus in the
Lateralization in manatees 81 nucleus is greatly expanded and appears to have overtaken the lateral geniculate nucleus and the lateral posterior nucleus, the thalamic nuclei assoc iated with vision. These results support the great importance of somatosensation in the Florida manatee (Sarko, Johnson, Switzer, Welker, & Reep, 2007). Manatees possess seven subnuclei in the facial motor nucleus (FMN), which may correspond to their spec ialized facial vibrissae (Marshall, Vaughn, Sarko, & Reep, 2007). The FMN is located in the same area as in other mammals, ventrally in the brainstem, ventrolateral to the pontine tegmentum and rostral to the inferior olive. The researchers identified seve n subnuclei, which were relatively large compared to the volume of the medulla. The nuclei were identified as follows: Medial and lateral, dorsolateral, ventrolateral, dorsointermediate, ventrointermediate, dorsomedial, and ventromedial subnuclei. The FMN was qualitatively large compared to the medullar volume and brain size. The large FMN and numerous well defined subnuclei are concomitant with the specializations of the vibrissae in the Florida manatee. These results suggest that therian mammals with spec ialized facial musculature and mystacial vibrissae possess larger and more subdivided facial motor nuclei. Despite what is known about the brain of the manatee, the organization of the hemispheres is not yet known. Using behavioral observations we can gat her information about possible hemispheric lateralization without invasive methods.