Context-dependent lateralization of trunk movements in wild Asian elephants

  • Andrey Giljov Department of Vertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation http://orcid.org/0000-0002-7533-1600
  • Shermin de Silva Elephant, Forest and Environment Conservation Trust, Sri Lanka, Colombo 5, 215 A 3/7 Park Road; Smithsonian Conservation Biology Institute, USA, VA 22630, Front Royal, 1500 Remount Rd http://orcid.org/0000-0001-5804-213X
  • Karina Karenina Department of Vertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaya nab., 7–9, Saint Petersburg, 199034, Russian Federation http://orcid.org/0000-0001-8200-6876

Abstract

Asymmetrical trunk use in elephants represents a distinctive example of motor lateralization. Previous studies have shown that trunk movements in the elephant behaviour associated with feeding is lateralized at the individual, but not the population level. The manifestation of lateralized behaviour depends on the nature of the behaviour and is usually more pronounced in social context. Therefore, we hypothesized that population-level lateralization of trunk use in elephants is manifested in social behaviour. One-sided biases in trunk movements were assessed in wild individually-identified Asian elephants during feeding (tearing off a tuft of grass) and social interactions (trunk-to-mouth contacts and trunk-to-genitals contacts between male initiator and female recipient). In feeding, lateralization at the individual and population levels was estimated based on 50 lateral trunk uses per individual. In social interactions, only the population-level bias was assessed using a single trunk contact from each individual. For trunk movements during feeding, elephants showed robust individual preferences, but no population-level lateralization. The distribution of right- and left-trunkers in the present study did not differ significantly from that obtained in previous studies of both the same elephant population and geographically distinct population. No population-level bias in trunk movements during trunk-to-mouth contacts was revealed. In trunk-to-genitals contacts, in contrast, a population-level lateralization was found. Right-sided trunk movements prevailed in males touching females. While individual preferences for feeding, combined with the absence of one-sided population bias, is obviously a species-typical characteristic of Asian elephants, social behaviour, such as male-female socio-sexual contacts, can elicit population-level lateralization of trunk use in this species. The right-sided bias in trunk-to-genitals contacts may reflect lateralization of olfactory perception. If this is the case, the revealed lateralization indicates a right-hemispheric advantage in the processing of social information which is consistent with the general tendency in mammals.

Keywords

laterality of trunk use, functional asymmetry of the trunk, trunk contacts, free-ranging Asian elephants, motor preferences, feeding, social laterality, lateralization of unpaired organs

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References

Afonso, D., Santana, C., and Rodriguez, M. 1993. Neonatal lateralization of behavior and brain dopaminergic asymmetry. Brain Research Bulletin 32(1):11–16. https://doi.org/10.1016/0361-9230(93)90312-Y

Arivazhagan, C., and Sukumar, R. 2008. Constructing age structures of Asian elephant populations: A comparison of two field methods of age estimation. Gajah 29:11–16.

Austin, N. P., and Rogers, L. J. 2012. Limb preferences and lateralization of aggression, reactivity and vigilance in feral horses, Equus caballus. Animal Behaviour 83(1):239–247. https://doi.org/10.1016/j.anbehav.2011.10.033

Bhavanani, A. B. Swarodaya Vigjnan. 2007. A scientific study of the nasal cycle. Yoga Mimamsa 39:32–38.

Bourne, V. J., and Todd, B. K. 2004. When left means right: An explanation of the left cradling bias in terms of right hemisphere specializations. Developmental Science, 7(1):19–24. https://doi.org/10.1111/j.1467-7687.2004.00318.x

Brancucci, A., Lucci, G., Mazzatenta, A., and Tommasi, L. 2009. Asymmetries of the human social brain in the visual, auditory and chemical modalities. Philosophical Transactions of the Royal Society of London B: Biological Sciences 364(1519):895–914. https://doi.org/10.1098/rstb.2008.0279

de Silva, S., Ranjeewa, A. D., and Weerakoon, D. 2011. Demography of Asian elephants (Elephas maximus) at Uda Walawe National Park, Sri Lanka based on identified individuals. Biological Conservation 144(5):1742–1752. https://doi.org/10.1016/j.biocon.2011.03.011

Denenberg, V. H., and Yutzey, D. A. 1985. Hemispheric laterality, behavioral asymmetry, and the effects of early experience in rats. In S. D. Glick (Ed), Cerebral lateralization in nonhuman species (pp. 109–133). Orlando, Fl: Academic Press

Espmark, Y., and Kinderås, K. 2002. Behavioural lateralisation in reindeer. Rangifer 22(1):51–59. https://doi.org/10.7557/2.22.1.687

Fernández-Carriba, S., Loeches, Á., Morcillo, A., and Hopkins, W. D. 2002. Asymmetry in facial expression of emotions by chimpanzees. Neuropsychologia 40(9):1523–1533. https://doi.org/10.1016/S0028-3932(02)00028-3

Forrester, G. S., Crawley, M., and Palmer, C. 2014a. Social environment elicits lateralized navigational paths in two populations of typically developing children. Brain and Cognition 91:21–27. https://doi.org/10.1016/j.bandc.2014.07.005

Forrester, G. S., Pegler, R., Thomas, M. S., and Mareschal, D. 2014b. Handedness as a marker of cerebral lateralization in children with and without autism. Behavioural Brain Research 268:14–21. https://doi.org/10.1016/j.bbr.2014.03.040

Forrester, G. S., Quaresmini, C., Leavens, D. A., Mareschal, D., and Thomas, M. S. 2013. Human handedness: an inherited evolutionary trait. Behavioural Brain Research 237:200–206. https://doi.org/10.1016/j.bbr.2012.09.037

Giljov, A., Karenina, K., Ingram, J., and Malashichev, Y. 2015. Parallel emergence of true handedness in the evolution of marsupials and placentals. Current Biology 25(14):1878–1884. https://doi.org/10.1016/j.cub.2015.05.043

Ghirlanda, S., Frasnelli, E., and Vallortigara, G. 2009. Intraspecific competition and coordination in the evolution of lateralization. Philosophical Transactions of the Royal Society of London B: Biological Sciences 364(1519):861–866. https://doi.org/10.1098/rstb.2008.0227

Ghirlanda, S., and Vallortigara, G. 2004. The evolution of brain lateralization: a game-theoretical analysis of population structure. Proceedings of the Royal Society of London B: Biological Sciences 271(1541):853–858. https://doi.org/10.1098/rspb.2003.2669

Grewal, R. 2010. The Book of Ganesha. London: Penguin.

Grimes, J. A. 1995. Ganapati: Song of the self. Albany: State University of New York Press.

Haakonsson, J. E., and Semple, S. 2009. Lateralization of trunk movements in captive Asian elephants (Elephas maximus). Laterality 14(4):413–422. https://doi.org/10.1080/13576500802572442

Hanbury, D. B., Edens, K. D., Bunch, D. A., Legg, C. E., and Watson, S. L. 2010. Multiple measures of laterality in Garnett’s bushbaby (Otolemur garnettii). American Journal of Primatology 72(3):206–216. https://doi.org/10.1002/ajp.20769

Harris, L. J. 1989. Footedness in parrots: three centuries of research, theory, and mere surmise. Canadian Journal of Psychology 43(3):369–396. https://doi.org/10.1037/h0084228

Hellige, J. B. 1993. Unity of thought and action: varieties of interaction between the left and right hemispheres. Current Directions in Psychological Science 2:21–25. https://doi.org/10.1111/1467-8721.ep10770559

Hook, M. A. 2004. The evolution of lateralized motor functions. In L. J. Rogers, and G. Kaplan (Eds.), Comparative vertebrate cognition (pp. 325–370). New York: Kluwer Academic / Plenum Publishing.

Hopkins, W. D., Russell, J. L., Remkus, M., Freeman, H., and Schapiro, S. J. 2007. Handedness and grooming in Pan troglodytes: comparative analysis between findings in captive and wild individuals. International Journal of Primatology 28(6):1315–1326. https://doi.org/10.1007/s10764-007-9221-x

Karenina, K., Giljov, A., Ingram, J., Rowntree, V. J., and Malashichev, Y. 2017. Lateralization of mother–infant interactions in a diverse range of mammal species. Nature Ecology & Evolution 1:0030. https://doi.org/10.1038/s41559-016-0030

Karenina, K. A., Giljov, A. N., and Malashichev, Y. B. 2013. Eye as a key element of conspecific image eliciting lateralized response in fish. Animal Cognition 16(2):287–300. https://doi.org/10.1007/s10071-012-0572-0

Keerthipriya, P., Tewari, R., and Vidya, T. N. C. 2015. Lateralization in trunk and forefoot movements in a population of free-ranging Asian elephants (Elephas maximus). Journal of Comparative Psychology 129(4):377–387. https://doi.org/10.1037/com0000013

Laska, M., and Tutsch, M. 2000. Laterality of tail resting posture in three species of New World primates. Neuropsychologia 38(7):1040–1046. https://doi.org/10.1016/S0028-3932(99)00147-5

Loizi, H., Goodwin, T. E., Rasmussen, L. E. L., Whitehouse, A. M., and Schulte, B. A. 2009. Sexual dimorphism in the performance of chemosensory investigatory behaviours by African elephants (Loxodonta africana). Behaviour 146(3):373–392. https://doi.org/10.1163/156853909X410964

Lorincz, E., and Fabre-Thorpe, M. 1996. Shift of laterality and compared analysis of paw performances in cats during practice of a visuomotor task. Journal of Comparative Psychology 110(3):307–315. https://doi.org/10.1037/0735-7036.110.3.307

MacNeilage, P. F., Rogers, L. J., and Vallortigara, G. 2009. Origins of the left & right brain. Scientific American 301(1):60–67. https://doi.org/10.1038/scientificamerican0709-60

Magat, M., and Brown, C. 2009. Laterality enhances cognition in Australian parrots. Proceedings of the Royal Society of London B: Biological Sciences 276(1676):4155–4162. https://doi.org/10.1098/rspb.2009.1397

Makecha, R., Fad, O., and Kuczaj II, S. A. 2012. The Role of Touch in the Social Interactions of Asian Elephants (Elephas maximus). International Journal of Comparative Psychology 25(1):60–82.

Malashichev, Y. B. 2006. One-sided limb preference is linked to alternating-limb locomotion in anuran amphibians. Journal of Comparative Psychology 120(4):401–410. https://doi.org/10.1037/0735-7036.120.4.401

Mangalam, M., Desai, N., and Singh, M. 2014. Division of labor in hand usage in free-ranging bonnet macaques, Macaca radiata. American Journal of Primatology 76(6):576–585. https://doi.org/10.1002/ajp.22250

Martin, F., and Niemitz, C. 2003. “Right-trunkers” and” left-trunkers”: side preferences of trunk movements in wild Asian elephants (Elephas maximus). Journal of Comparative Psychology 117(4):371–379. https://doi.org/10.1037/0735-7036.117.4.371

McGreevy, P. D., and Rogers, L. J. 2005. Motor and sensory laterality in thoroughbred horses. Applied Animal Behaviour Science 92(4):337–352. https://doi.org/10.1016/j.applanim.2004.11.012

McGrew, W. C., and Marchant, L. F. 1999. Laterality of hand use pays off in foraging success for wild chimpanzees. Primates 40(3):509–513. https://doi.org/10.1007/BF02557586

Meguerditchian, A., Vauclair, J., and Hopkins, W. D. 2013. On the origins of human handedness and language: a comparative review of hand preferences for bimanual coordinated actions and gestural communication in nonhuman primates. Developmental Psychobiology 55(6):637–650. https://doi.org/10.1002/dev.21150

Mutha, P. K., Haaland, K. Y., and Sainburg, R. L. 2013. Rethinking motor lateralization: specialized but complementary mechanisms for motor control of each arm. PLoS ONE 8(3):e58582. https://doi.org/10.1371/journal.pone.0058582

Nudo, R. J., Jenkins, W. M., Merzenich, M. M., Prejean, T., and Grenda, R. 1992. Neurophysiological correlates of hand preference in primary motor cortex of adult squirrel monkeys. Journal of Neuroscience 12(8):2918–2947.

Perelle, I. B., and Ehrman, L. 1994. An international study of human handedness: the data. Behavior Genetics 24(3):217–227. https://doi.org/10.1007/BF01067189

Phillips, K. A., Schaeffer, J., Barrett, E., and Hopkins, W. D. 2013. Performance asymmetries in tool use are associated with corpus callosum integrity in chimpanzees (Pan troglodytes): a diffusion tensor imaging study. Behavioral Neuroscience 127(1):106–113. https://doi.org/10.1037/a0031089

Poyser, F., Caldwell, C., and Cobb, M. 2006. Dog paw preference shows lability and sex differences. Behavioural Processes 73(2):216–221. https://doi.org/10.1016/j.beproc.2006.05.011

Prieur, J., Pika, S., Barbu, S., and Blois-Heulin, C. 2016a. A multifactorial investigation of captive chimpanzees’ intraspecific gestural laterality. Animal Behaviour 116:31–43. https://doi.org/10.1016/j.anbehav.2016.03.024

Prieur, J., Pika, S., Barbu, S., and Blois-Heulin, C. 2016b. Gorillas are right-handed for their most frequent intraspecific gestures. Animal Behaviour 118:165–170. https://doi.org/10.1016/j.anbehav.2016.06.008

Quaranta, A., Siniscalchi, M., and Vallortigara, G. 2007. Asymmetric tail-wagging responses by dogs to different emotive stimuli. Current Biology 17(6):R199–R201. https://doi.org/10.1016/j.cub.2007.02.008

Quaresmini, C., Forrester, G. S., Spiezio, C., and Vallortigara, G. 2014. Social environment elicits lateralized behaviors in gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes). Journal of Comparative Psychology 128(3):276–284. https://doi.org/10.1037/a0036355

Racine, R. A. 1980. Behavior associated with feeding in captive African and Asian elephants. Elephant (Supplement) 1:57–71.

Rasmussen, L. E. L., and Schulte, B. A. 1998. Chemical signals in the reproduction of Asian (Elephas maximus) and African (Loxodonta africana) elephants. Animal Reproduction Science 53(1):19–34. https://doi.org/10.1016/S0378-4320(98)001249

Reimchen, T. E., and Spoljaric, M. A. 2011. Right paw foraging bias in wild black bear (Ursus americanus kermodei). Laterality 16:471–478. https://doi.org/10.1080/1357650X.2010.485202

Rogers, L. J. 2009. Hand and paw preferences in relation to the lateralized brain. Philosophical Transactions of the Royal Society of London B: Biological Sciences 364(1519):943–954. https://doi.org/10.1098/rstb.2008.0225

Rogers, L. J., and Kaplan, G. 1996. Hand preferences and other lateral biases in rehabilitated orang-utans, Pongo pygmaeus pygmaeus. Animal Behaviour 51(1):13–25. https://doi.org/10.1006/anbe.1996.0002

Rogers, L .J., and Vallortigara, G. 2017. Lateralized brain functions: methods in human and non-human species. New York: Springer.

Rogers, L. J., Vallortigara, G., and Andrew, R. J. 2013. Divided brains: the biology and behaviour of brain asymmetries. Cambridge: Cambridge University Press.

Rosa Salva, O., Regolin, L., Mascalzoni, E., and Vallortigara, G. 2012. Cerebral and behavioural asymmetries in animal social recognition. Comparative Cognition & Behavior Reviews 7:110–138. https://doi.org/10.3819/ccbr.2012.70006

Royet, J. P., and Plailly, J. 2004. Lateralization of olfactory processes. Chemical Senses 29(8):731–745. https://doi.org/10.1093/chemse/bjh067

Sakai, M., Hishii, T., Takeda, S., and Kohshima, S. 2006. Laterality of flipper rubbing behaviour in wild bottlenose dolphins (Tursiops aduncus): Caused by asymmetry of eye use?. Behavioural Brain Research 170(2):204–210. https://doi.org/10.1016/j.bbr.2006.02.018

Shabbott, B. A., and Sainburg, R. L. 2008. Differentiating between two models of motor lateralization. Journal of Neurophysiology 100(2):565–575. https://doi.org/10.1152/jn.90349.2008

Shoshani, J. 1998. Understanding proboscidean evolution: a formidable task. Trends in Ecology & Evolution 13(12):480–487. https://doi.org/10.1016/S0169-5347(98)01491-8

Shoshani, J., Kupsky, W. J., and Marchant, G. H. 2006. Elephant brain: Part I: Gross morphology, functions, comparative anatomy, and evolution. Brain Research Bulletin 70(2):124–157. https://doi.org/10.1016/j.brainresbull.2006.03.016

Siniscalchi, M. 2017. Olfactory lateralization. In L. Rogers, and G. Vallortigara (Eds.), Lateralized brain functions: methods in human and non-human species (pp. 103–120). New York: Springer.

Siniscalchi, M., and Quaranta, A. 2014. Wagging to the right or to the left: lateralization and what it tells of the dog’s social brain. In J. Kaminski, and S. Marshall-Pescini (Eds.), The social dog: behavior and cognition (pp. 373–393). Amsterdam: Elsevier.

Siniscalchi, M., Dimatteo, S., Pepe, A. M., Sasso, R., and Quaranta, A. 2012. Visual lateralization in wild striped dolphins (Stenella coeruleoalba) in response to stimuli with different degrees of familiarity. PLoS ONE, 7(1):e30001. https://doi.org/10.1371/journal.pone.0030001

Siniscalchi, M., Padalino, B., Aubé, L., and Quaranta, A. 2015. Right-nostril use during sniffing at arousing stimuli produces higher cardiac activity in jumper horses. Laterality 20(4):483–500. https://doi.org/10.1080/1357650X.2015.1005629

Ströckens, F., Güntürkün, O., and Ocklenburg, S. 2013. Limb preferences in non-human vertebrates. Laterality 18(5):536–575. https://doi.org/10.1080/1357650X.2012.723008

Thitaram, C., Chansitthiwet, S., Pongsopawijit, P., Brown, J. L., Wongkalasin, W., Daram, P., … and Colenbrander, B. 2009. Use of genital inspection and female urine tests to detect oestrus in captive Asian elephants. Animal Reproduction Science 115(1):267–278. https://doi.org/10.1016/j.anireprosci.2008.11.017

Tyler-Julian, K., Chapman, K. M., Frances, C., and Bauer, G. B. 2016. Behavioral lateralization in the Florida manatee (Trichechus manatus latirostris). International Journal of Comparative Psychology 29:1–13.

Varma, S., Baskaran, N., and Sukumar, R. 2012. Field key for elephant population estimation and age and sex classification. Bangalore, Karnataka: Asian Nature Conservation Foundation, Innovation Centre, Indian Institute of Science and Centre for Ecological Sciences.

Vidya, T. N. C., Prasad, D., and Ghosh, A. 2014. Individual identification in Asian elephants. Gajah 40:3–17.

Wells, D. L. 2003. Lateralised behaviour in the domestic dog, Canis familiaris. Behavioural Processes 61(1):27–35. https://doi.org/10.1016/S0376-6357(02)00161-4

Yasui, S., and Idani, G. I. 2017. Social significance of trunk use in captive Asian elephants. Ethology Ecology & Evolution 29(4):330–350. https://doi.org/10.1080/03949370.2016.1179684
Published
2017-09-01
How to Cite
GILJOV, Andrey; DE SILVA, Shermin; KARENINA, Karina. Context-dependent lateralization of trunk movements in wild Asian elephants. Biological Communications, [S.l.], v. 62, n. 2, p. 82–92, sep. 2017. ISSN 2587-5779. Available at: <https://biocomm.spbu.ru/article/view/11>. Date accessed: 17 jan. 2018. doi: https://doi.org/10.21638/11701/spbu03.2017.204.
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