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Pattern of Lateralized Behaviors in a Caudate Amphibian, Ambystoma mexicanum

Evgeny I. Izvekov, Vera V. Pavlova, Ekaterina M. Ognevaja, Valentin A. Nepomnyashchikh, Yegor Malashichev

Abstract


Laterality of brain and behavior at the individual and/or group level is a characteristic of all vertebrate classes. The general pattern of left-right asymmetry in vertebrates is so that left-eye/right-hemisphere system is used to detect socially important images, like conspecifics, and also recognize danger, while the right-eye/left-hemisphere system is used to discriminate prey and food items from inedible objects. However, the pattern of motor and visual lateralization in caudate amphibians is poorly investigated to date. Here we present the first evidence of individual and group level motor and visual lateralization in sexually mature and immature larvae of the Mexican axolotl, Ambystoma mexicanum, thus presenting a comprehensive characteristic of the lateralized behavioral pattern in a salamander species. First, we performed four successive tests to assess asymmetry in rapid C-start and measure its characteristics in responses to startle stimuli in sexually immature larvae. We experimentally showed that axolotls exhibited a leftward population bias in each of four C-start tests, of which the bias was significant in the second test and in the pooled data for all four tests. Second, in mature axolotls we have found right-sided individual level asymmetry and, at the group level, a tendency to react more actively to food items (live chironomid larvae) appeared in their right visual hemifield. Third, individual axolotl larvae been placed in the square aquarium with two opposite mat walls and two opposite mirror walls preferred to stay near to mirror walls, rather than near to mat walls. At the group level, this preference increased over three successive tests and reached significance in the third test and in the pooled data. At both individual and group levels axolotls showed statistically significant lateralization, preferring to inspect the mirror walls with their left eyes in all three tests. Overall, the expressed pattern of lateralization in the Mexican axolotl corresponds to the general pattern of lateralization established for other vertebrates including anuran amphibians.


Keywords


Axolotl; Ambystoma mexicanum; caudate amphibians; C-start; escape response; reaction to food; response to mirror; left−right asymmetry; behavioral lateralization.

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Andrew R. J. and Dharmaretnam M. A. (1991), «A timetable of development», in: Neural and Behavioural Plasticity: The Use of the Chick as a Model, Oxford, pp. 166 – 176.

Azizi E. and Landberg T. (2002), «Effects of metamorphosis on the aquatic escape response of the two-lined salamander (Eurycea bislineata)», J. Exp. Biol., 205, 841 – 849.

Bisazza A., Cantalupo C., Capocchiano M., and Vallortigara G. (2000), «Population lateralization and social behavior: A study with sixteen species of fish», Laterality, 3, 269 – 284.

Bisazza A., De Santi A., Bonso S., and Sovrano V. A. (2002), «Frogs and toads in front of a mirror: lateralization of response to social stimuli in tadpoles of five anuran species», Behav. Brain Res., 134, 417 – 424.

Bonati B., Csermely D., and Romani R. (2008), «Lateralization in the predatory behavior of the common wall lizard (Podarcis muralis)», Behav. Proc., 79(3), 171 – 174.

Fitzpatrick B., Benard M. F., and Fordyce J. A. (2003), «Morphology and escape performance of tiger salamander larvae (Ambystoma tigrinum mavortium)», J. Exp. Zool., 297A, 147 – 159.

Giljov A., Karenina K., and Malashichev Y. (2009), «An eye for a worm: Lateralisation of feeding behavior in aquatic anamniotes», Laterality, 14(3), 273 – 286.

Green A. (1997), «Asymmetrical turning during spermatophore transfer in the male smooth newts», Animal Behav., 54(2), 343 – 348.

Hoffman A. M., Robakiewicz P. E., Tuttle E. M., and Rogers L. J. (2006), «Behavioural lateralisation in the Australian magpie (Gymnorhina tibicen)», Laterality, 11, 110 – 121.

Karenina K., Giljov A., and Malashichev Y. (2013), «Eye as key element of conspecific image eliciting lateralized response in fish», Animal Cognition, 16, 287 – 300.

Karenina K., Giljov A., Ingram J., Rowntree V., and Malashichev Y. (2017), «Lateralization of mother-infant interactions in a diverse range of mammal species», Nature Ecol. Evol., 1, 0030.

Lippolis G., Joss J. M. P., and Rogers L. J. (2009), «Australian Lungfish (Neoceratodus forsteri): A Missing Link in the Evolution of Complementary Side Biases for Predator Avoidance and Prey Capture», Brain Behav. Evol., 73, 295 – 303.

Malashichev Y. B. and Deckel A. W. (eds.) (2006), Behavioral and Morphological Asymmetries in Vertebrates, Landes Biosciences, Georgetown (TX), pp. 1 – 193.

Marzona E. and Giacomo C. (2002), «Display lateralization in the courtship behaviour of the alpine newt (Triturus alpestris)», Laterality, 7(3), 285 – 296.

Mikhailova G. Z., Pavlik V. D., Tiras N. R., and Moshkov D. A. (2005a), «Correlation of the sizes of Mauthner neurons with the preference in the goldfish to turn rightwards or leftwards», Morphologia, 127(2), 16 – 19.

Mikhailova G. Z., Arutyunyan A. V., Santalova I. M., Pavlik V. D., Tiras N. P., and Moshkov D. A. (2005b), «Asymmetry of motor behavior of the goldfish in a narrow channel», Neurophysiology, 37(1), 52 – 60.

Miklosi A. and Andrew R. J. (1999), «Right eye use associated with decision to bite in zebrafish», Behav. Brain Res., 105, 199 – 205.

Miklosi A., Andrew R. J., and Gasparini S. (2001), «Role of right hemifield in visual control of approach to target in zebrafish», Behav. Brain Res., 122, 57 – 65.

Nagy M., Akos Z., Biro D., and Vicsek T. (2010), «Hierarchical group dynamics in pigeon flocks», Nature, 464, 890 – 893. (arXiv: 1010.5394v1 [physics.bio-ph])

Robins A., Chen P., Beazley L. D., and Dunlop S. A. (2005), «Lateralized predatory responses in the Ornate dragon lizard (Ctenophorus ornatus)», Neuroreport, 16, 849 – 852.

Robins A. and Rogers L. J. (2004), «Lateralized prey-catching responses in the cane toad Bufo marinus: analysis of complex visual stimuli», Animal Behav., 68, 567 – 575.

Robins A. and Rogers L. J. (2006a), «Complementary and lateralized forms of processing in Bufo marinus for novel and familiar prey», Neurobiol. Learning Memory, 86, 214 – 227.

Robins A. and Rogers L. J. (2006b), «Lateralized visual and motor responses in the green tree frog, Litoria caerulea», Animal Behav., 72, 843 – 852.

Rock M. K., Hackett J. T., and Brown D. L. (1981), «Does the Mauthner cell conform to the criteria of the command neuron concept?» Brain Res., 204(1), 21 – 27.

Rogers L. J., Vallortigara G., and Andrew R. J. (2013), Divided Brains. The Biology and Behaviour of Brain Asymmetries, Cambridge Univ. Press, Cambridge.

Ryugo D. K., Wu M. M., and Pongstaporn T. (1996), «Activity-related features of synapse morphology: a study of end bulbs of Held», J. Compar. Neurol., 365(3), 141 – 158.

Shtanchayev R. Sh., Mikhailova G. Z., Dektyaryova N. Yu., Kokanova N. A., and Moshkov D. A. (2007), «Changes of the ventral dendrite of goldfish Mauthner neuron induced by optokinetic stimulation», Morphologia, 132(6), 29 – 34.

Sokal R. R. and Rohlf F. J. (1995), Biometry. 3rd Edition, W. H. Freeman and Company, New York.

Sovrano V., Bisazza A., and Vallortigara G. (2001), «Lateralization of response to social stimuli in fishes: A comparison between different methods and species», Physiol. Behav., 74, 237 – 244.

Sovrano V. A., Quaresmini C., and Stancher G. (2017), «Tortoises in front of mirrors: Brain asymmetries and lateralized behaviors in the tortoise (Testudo hermanni)», Behav. Brain Res., in press. DOI: 10.1016/j.bbr.2017.06.021.

Sovrano V., Rainoldi C., Bisazza A., and Vallortigara G. (1999), «Roots of brain specializations: preferential left-eye use during mirro-image inspection in six species of teleost fish», Behav. Brain Res., 106, 175 – 180.

Vallortigara G., Rogers L. J., Bisazza A., Lippolis G., and Robins A. (1998), «Complementary right and left hemifield use for predatory and agonistic behavior in toads», Neuroreport, 9, 3341 – 3344.

Wassersug R. J. and Hoff K. (1985), «The kinematics of swimming in anuran larvae», J. Exp. Biol., 119, 1 – 30.

Wassersug R. L. and Yamashita M. (2002), «Assessing and interpreting lateralised behaviours in anuran larvae», Laterality, 7(3), 241 – 260.

Will U. (1991), «Amphibian Mauthner cells», Brain Behav. Evol., 37, 317 – 332.

Wilson R. S. and Franklin C. E. (2000), «Effect of ontogenetic increases in body size on burst swimming performance in tadpoles of the striped marsh frog, Limnodynastes peronei», Physiol. Biochem. Zool., 73(2), 142 – 152.

Yamashita M., Naitoh T., and Wassersug R. J. (2000), «Startle response and turning bias in Microhyla tadpoles», Zool. Sci., 17, 185 – 189.


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