Abstract
This chapter discusses the methods of studying behavioral lateralization in invertebrate animals. Although to date not a great deal is known about lateralized behavior and cognitive function in invertebrates, a number of studies have provided evidence of lateralization in a range of invertebrate species. Behavioral asymmetries have been shown in phyla such as Arthropoda (Insecta, Arachida, and Malacostraca), Mollusca (Gastropoda and Cephalopoda) and Nematoda, and in a variety of behaviors. Here I report the findings of research conducted on lateralization in invertebrates with a specific focus on the methodology adopted. Behavioral asymmetries in the invertebrate line have been investigated by observing biases in different types of behavior that can be classified in six main groups corresponding to the six sections of the chapter (summarized in Table 1). These six sections analyze the methods used to investigate lateral biases in (1) catching prey and foraging behavior; (2) escape response; (3) interactions with conspecifics (aggressive and sexual behavior); (4) spontaneous motor behavior (preferential choice in a T-maze); (5) sensory modalities (olfaction, vision, and hearing); and (6) recall of memory associated with conditioning in one of these sensory modalities. For each method the advantages and disadvantages of using it are examined and the main findings are reported and discussed.
Key words
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
McManus IC (1999) Handedness, cerebral lateralisation and the evolution of language. In: Corballis MC, Lea SEG (eds) The descent of mind: psychological perspective on hominid evolution. Oxford University Press, Oxford
Rogers LJ, Vallortigara G, Andrew R (2013) Divided brains: the biology and behaviour of brain asymmetries. Cambridge University Press, Cambridge
Versace E, Vallortigara G (2015) Forelimb preferences in human beings and other species: multiple models for testing hypotheses on lateralization. Front Psychol 6:233
Dadda M, Koolhaas WH, Domenici P (2010) Behavioural asymmetry affects escape performance in a teleost fish. Biol Lett 6:414–417
Rogers LJ (2002) Lateralized brain function in anurans: comparison to lateralization in other vertebrates. Laterality 7:219–239
Kight SL, Steelman L, Coffey G, Lucente J, Castillo M (2008) Evidence of population level in giant water bugs, Belostoma flumineum Say (Heteroptera: Belostomatidae): T-maze turning is left biased. Behav Proc 79:66–69
Lippolis G, Joss J, Rogers LJ (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
Tommasi L, Andrew RJ, Vallortigara G (2000) Eye use is determined by the nature of task in the domestic chick (Gallus gallus). Behav Brain Res 112:119–126
Rogers LJ, Kaplan G (2006) An eye for a predator: lateralization in birds, with particular reference to the Australian magpie. In: Malashichev Y, Deckel W (eds) Behavioral and morphological asymmetries in vertebrates. Landes Bioscience, TX, pp 47–57
Vallortigara G, Rogers LJ, Bisazza A, Lippolis G, Robins A (1998) Complementary right and left hemifield use for predatory and agonistic behaviour in toads. NeuroReport 9:3341–3344
Robins R, Rogers LJ (2006) Complementary and lateralized forms of processing in Bufo marinus for novel and familiar prey. Neurobiol Learn Mem 86:214–227
Vallortigara G, Rogers LJ (2005) Survival with an asymmetrical brain: advantages and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–633
Frasnelli E, Vallortigara G, Rogers LJ (2012) Left-right asymmetries of behavioural and nervous system in invertebrates. Neurosci Biobehav Rev 36:1273–1291
Frasnelli E (2013) Brain and behavioral lateralization in invertebrates. Front Psychol 4(939):1–10
Rogers LJ (2014) Asymmetry of brain and behavior in animals: its development, function, and human relevance. Genesis 52(6):555–571
Vallortigara G, Versace E (2015) Laterality at the neural, cognitive and behavioural levels. In: Snowdon C, Burghardt G, Pepperberg I, Call J, Zentall T (eds) APA handbook of comparative psychology. American Psychological Association Press, Washington, DC
Heuts BA, Brunt T (2005) Behavioural left-right asymmetry extends to arthropods. Behav Brain Sci 28:601–602
Hönicke C, Bliss P, Moritz RF (2015) Effect of density on traffic and velocity on trunk trails of Formica pratensis. Sci Nat 102(3–4):17
Frasnelli E, Iakovlev I, Reznikova Z (2012) Asymmetry in antennal contacts during trophallaxis in ants. Behav Brain Res 32:7–12
Reznikova Z (2007) Animal intelligence: from individual to social cognition. Cambridge University Press, Cambridge
Heuts BA, Lambrechts DYM (1999) Positional biases in leg loss of spiders and harvestmen (Arachnida). Entomol Ber (Amst) 59:13–20
Ades C, Ramires EN (2002) Asymmetry of leg use during prey handling in the spider Scytodes globula (Scytodidae). J Insect Behav 15:563–570
Ramires EN (1999) Uma abordagem comparativa ao comportamento defensivo, agonístico e locomotor de três espécies de aranhas do gênero Loxosceles (Sicariidae). Unpublished doctoral dissertation, Institute of Psychology, University of São Paulo, Brazil
Kells AR, Goulson D (2001) Evidence for handedness in bumblebees. J Insect Behav 14:47–55
Kawaguchi LG, Ohashi K, Toquenaga Y (2007) Contrasting responses of bumble bees to feeding conspecifics on their familiar and unfamiliar flowers. Proc R Soc B 274:2661–2667
Leadbeater E, Chittka L (2008) Social transmission of nectar-robbing behaviour in bumble-bees. Proc R Soc B 275:1669–1674
Goulson D, Park KJ, Tinsley MC, Bussière LF, Vallejo-Marin M (2013) Social learning drives handedness in nectar robbing bumblebees. Behav Ecol Sociobiol 67:1141–1150
Wells MJ (1978) Octopus: physiology and behaviour of an advanced invertebrate. Chapman & Hall, London
Wells MJ (1962) Brain and behaviour in cephalopods. Heinemann, London
Muntz WRA (1963) Interocular transfer and the function of the optic lobes in octopus. Q J Exp Psychol 15:116–124
Byrne RA, Kuba M, Griebel U (2002) Lateral asymmetry of eye use in Octopus vulgaris. Anim Behav 64:461–468
Byrne RA, Kuba MJ, Meisel DV (2004) Lateralized eye use in Octopus vulgaris shows antisymmetrical distribution. Anim Behav 68:1107–1114
Frasnelli E, Ponte G, Fiorito G, Vallortigara G (2014) Investigating lateralization in octopuses: first evidence of asymmetry in the optic lobes. In: Fourth workshop on cognition and evolution, Rovereto, Italy
Byrne RA, Kuba MJ, Meisel DV, Griebel U, Mather JA (2006) Does Octopus vulgaris have preferred arms? J Comp Psychol 3:198–204
Byrne RA, Kuba MJ, Meisel DV, Griebel U, Mather JA (2006) Octopus arm choice is strongly influenced by eye use. Behav Brain Res 172:195–201
Fagot J, Vauclair J (1991) Manual laterality in non human primates: a distinction between handedness and manual specialization. Psychol Bull 109:76–89
Gutnick T, Byrne RA, Hochner B, Kuba M (2011) Octopus vulgaris uses visual information to determine the location of its arm. Curr Biol 21:460–462
Heuts BA (1999) Lateralization of trunk muscle volume, and lateralization of swimming turns of fish responding to external stimuli. Behav Processes 47:113–124
Bisazza A, Rogers LJ, Vallortigara G (1998) The origins of cerebral asymmetry: a review of evidence of behavioural and brain lateralization in fishes, amphibians, and reptiles. Neurosci Biobehav Rev 22:411–426
Bisazza A, De Santi A, Vallortigara G (1999) Laterally and cooperation: mosquitofish move closer to a predator when the companion is on the left side. Anim Behav 57:1145–1149
Vallortigara G, Bisazza A (2002) How ancient is brain lateralization? In: Andrew RJ, Rogers LJ (eds) Comparative vertebrate lateralization. Cambridge University Press, Cambridge, pp 9–69
Vallortigara G, Rogers LJ, Bisazza A (1999) Possible evolutionary origins of cognitive brain lateralization. Brain Res Rev 30:164–175
Takeuchi Y, Tobo S, Hori M (2008) Morphological asymmetry of the abdomen and behavioral laterality in atyid shrimps. Zool Sci 25:355–363
Tobo S, Takeuchi Y, Hori M (2011) Morphological asymmetry and behavioural laterality in the crayfish, Procambarus clarkia. Ecol Res 27(1):53–59
Rosa Salva O, Regolin L, Mascalzoni E, Vallortigara G (2012) Cerebral and behavioural asymmetry in animal social recognition. Comp Cogn Behav Rev 7:110–138
Hews DK, Castellano M, Hara E (2004) Aggression in females is also lateralized: left-eye bias during aggressive courtship rejection in lizards. Anim Behav 68:1201–1207
Ventolini N, Ferrero EA, Sponza S et al (2005) Laterality in the wild: preferential hemifield use during predatory and sexual behaviour in the black-winged stilt. Anim Behav 69:1077–1084
Austin NA, Rogers LJ (2012) Limb preference and lateralization of aggression, reactivity and vigilance in feral horses (Equus caballus). Anim Behav 83:239–247
Casperd JM, Dunbar RIM (1996) Asymmetries in the visual processing of emotional cues during agonistic interactions in gelada baboons. Behav Processes 37:57–65
Pratt AE, McLain DK, Lathrop GR (2003) The assessment game in sand fiddler crab contests for breeding burrows. Anim Behav 65:945–955
Jones DS, George RW (1982) Handedness in fiddler crabs as an aid in taxonomic grouping of the genus Uca (Decapoda, Ocypodidae). Crustaceana 43:100–102
Backwell PRY, Matsumasa M, Double M, Roberts A, Murai M, Keogh JS, Jennions MD (2007) What are the consequences of being left-clawed in a predominantly right-clawed fiddler crab? Proc R Soc B 274:2723–2729
Salmon M (1984) The courtship, aggressive and mating system of a “primitive” fiddler crab (Uca vocans). Trans Zool Soc Lond 37:1–50
Hyatt GW, Salmon M (1978) Combat in fiddler crabs Uca pugilator and Uca pugnax-quantitative analysis. Behaviour 65:182–211
Rogers LJ, Rigosi E, Frasnelli E, Vallortigara G (2013) A right antenna for social behaviour in honeybees. Sci Rep 3:2045
Rogers LJ, Frasnelli E, Versace E, Vallortigara G (2016) Lateralized social behaviour in a “solitary” red mason bee, Osmia bicornis. Sci Rep 6:29411. doi:10.1038/srep29411
Nepi M, Cresti L, Maccagnani B, Ladurner E, Pacini E (2005) From the anther to the proctodeum: Pear (Pyrus communis) pollen digestion in Osmia cornuta larvae. J Insect Physiol 51:749–757
Tepedino VJ, Torchio PF (1994) Founding and ussuroing: equally efficient paths to nesting success in Osmia lignaria propinqua (Hymenoptera: Megachilidae). Ann Entomol Soc Am 87:946–953
Seidelmann K (1999) The race for females: the mating system of the red mason bee, Osmia rufa (L.) (Hymenoptera: Megachilidae). J Insect Behav 12:13–25
Benelli G, Donati E, Romano D, Stefanini C, Messing RH, Canale A (2015) Lateralization of aggressive displays in a tephritid fly. Sci Nat Naturwiss 102(1–2):1251
Benelli G, Romano D, Messing RH, Canale A (2015) Population-level lateralized aggressive and courtship displays make better fighters not lovers: evidence from a fly. Behav Processes 115:163–168
Shelly TE (2000) Aggression between wild and laboratory-reared sterile males of the Mediterranean fruit fly in a natural habitat (Diptera: Tephritidae). Fla Entomol 83:105–108
Papadopoulos NT, Carey JR, Liedo P, Muller G, Senturk D (2009) Virgin females compete for mates in the male lekking species Ceratitis capitata. Physiol Entomol 34:238–245
Romano D, Canale A, Benelli G (2015) Do right-biased boxers do it better? Population-level asymmetry of aggressive displays enhances fighting success in blowflies. Behav Processes 113C:159–162
Benelli G, Romano D, Messing RH, Canale A (2015) First report of behavioural lateralisation in mosquitoes: right-biased kicking behaviour against males in females of the Asian tiger mosquito, Aedes albopictus. Parasitol Res 114:1613–1617
Asami T, Gitternberger E, Falkner G (2008) Whole-body enantiomorphy and maternal inheritance of chiral reversal in the pond snail Lymnaea stagnalis. J Heredity 99(5):552–557
Davison A, Frend HT, Moray C, Wheatley H, Searle LJ, Eichhorn MP (2009) Mating behaviour in pond snails Lymnaea stagnalis is a maternally inherited lateralized trait. Biol Lett 5:20–22
Van Duivenboden YA, Ter Maat A (1988) Mating behaviour of Lymnaea stagnalis. Malacologia 28:53–64
Chase R (1986) Brain cells that command sexual behavior in the snail Helix aspersa. J Neurobiol 17(6):669–679
Kamimura Y (2006) Right-handed penises of the earwig Labidura riparia (Insecta, Dermaptera, Labiduridae): evolutionary relationships between structural and behavioral asymmetries. J Morphol 267:1381–1389
Regen J (1913) Ueber die Anlockung des Weibchens von Gryllus campestris L. durch telephonisch uebertragene Stridulationslaute des Maennchens. Pfliigers Arch 155:193–200
Elliott CJH, Koch UT (1983) Sensory feedback stabilizing reliable stridulation in the field cricket Glyllus campestris L. Anim Behav 31:887–901
Stärk AA (1958) Untersuchungen am Lautorgan einiger Grillen- und Laubheuschrecken-Arten, zugleich ein Beitrag zum Rechts-Links-Problem. Zool Jahrb Anat 77:9–50
Olton DS (1979) Mazes, maps, and memory. Am Psychol 34:583–596
O'Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34(1):171–175
Alves C, Chichery R, Boal JG, Dickel L (2007) Orientation in the cuttlefish Sepia officinalis: response versus place learning. Anim Cogn 10:29–36
Jozet-Alves C, Viblanc VA, Romagny S, Dacher M, Healy SD, Dickel L (2012) Visual lateralization is task- and age-dependent in cuttlefish (Sepia officinalis). Anim Behav 83:1313–1318
Jozet-Alves C, Romagny S, Bellanger C, Dickel L (2012) Cerebral correlates of visual lateralization in Sepia. Behav Brain Res 234:20–25
Nixon M, Young JZ (2003) The brains and lives of cephalopods. Oxford University Press, Oxford
Jozet-Alves C, Hébert M (2013) Embryonic exposure to predator odour modulates visual lateralization in cuttlefish. Proc R Soc B 280(1752):2012–2575
Hunt ER, O'Shea-Wheller TA, Albery GF, Bridger TH, Gumn M, Franks NR (2014) Ants show a leftward turning bias when exploring unknown nest sites. Biol Lett 10(12):20140945
Cooper R, Nudo N, Gonzales JM, Vinson SB, Liang H (2010) Side-dominance of Periplaneta americana persists through antenna amputation. J Insect Behav 24:175–185
Buchanan SM, Kain JS, de Bivort BL (2015) Neuronal control of locomotor handedness in Drosophila. Proc Natl Acad Sci U S A 112(21):6700–6705
Bell ATA, Niven JE (2014) Individual-level, context-dependent handedness in the desert locust. Curr Biol 24:R382–R383
Letzkus P, Ribi WA, Wood JT, Zhu H, Zhang SW, Srinivasan MV (2006) Lateralization of olfaction in the honeybee Apis mellifera. Curr Biol 16:1471–1476
Bitterman ME, Menzel R, Fietz A, Schafer S (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J Comp Psychol 97:107–119
Frasnelli E, Anfora G, Trona F, Tessarolo F, Vallortigara G (2010) Morpho-functional asymmetry of the olfactory receptors of the honeybee (Apis mellifera). Behav Brain Res 209:221–225
Letzkus P, Boeddeker N, Wood JT, Zhang SW, Srinivasan MV (2007) Lateralization of visual learning in the honeybee. Biol Lett 4:16–18
Hori S, Takeuchi H, Arikawa K, Kinoshita M, Ichikawa N, Sasaki M, Kubo T (2006) Associative visual learning, color discrimination, and chromatic adaptation in the harnessed honeybee Apis mellifera L. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192:691–700
Basari N, Bruendl AC, Hemingway CE, Roberts NW, Sendova-Franks AB, Franks NR (2014) Landmarks and ant search strategies after interrupted tandem runs. J Exp Biol 217:944–954
Möglich M (1978) Social organization of nest emigration in Leptothorax (Hym., Form.). Insectes Soc 25:205–225
Tommasi L, Vallortigara G (2001) Encoding of geometric and landmark information in the left and right hemispheres of the avian brain. Behav Neurosci 115:602–613
Duistermars BJ, Chow DM, Frye MA (2009) Flies require bilateral sensory input to track odour gradients in flight. Curr Biol 19:1301–1307
Louis M, Huber T, Benton R, Sakmar TP, Vosshall LB (2007) Bilateral olfactory sensory input enhances chemotaxis behavior. Nat Neurosci 11:87–199
Bailey WJ, Yang S (2002) Hearing asymmetry and auditory acuity in the Australian bushcricket Requena verticalis (Listroscelidinae; Tettigoniidae; Orthoptera). J Exp Biol 205:2935–2942
Prager J, Larsen ON (1981) Asymmetrical hearing in the water bug Corixa punctata observed with laser vibrometry. Naturwissenschaften 68:579–580
Prager J, Streng R (1982) The resonance properties of the physical gill of Corixa punctata and their significance in sound reception. J Comp Physiol A 148:323–335
Rogers LJ, Vallortigara G (2008) From antenna to antenna: lateral shift of olfactory memory in honeybees. PLoS One 3:e2340
Frasnelli E, Vallortigara G, Rogers LJ (2010) Response competition associated with right-left antennal asymmetries of new and old olfactory memory traces in honeybees. Behav Brain Res 209:36–41
Cipolla-Neto J, Horn G, McCabe BJ (1982) Hemispheric asymmetry and imprinting: the effect of sequential lesions of the hyperstriatum ventrale. Exp Brain Res 48:22–27
Clayton NS, Krebs JR (1994) Lateralization and unilateral transfer of spatial memory in marsh tits: are two eyes better than one? J Comp Physiol A 174:769–773
Andrew RJ (1999) The differential roles of right and left sides of the brain in memory formation. Behav Brain Res 98:289–295
Rigosi E, Frasnelli E, Vinegoni C, Antolini R, Anfora G, Vallortigara G, Haase A (2011) Searching for anatomical correlates of olfactory lateralization in the honeybee antennal lobes: a morphological and behavioural study. Behav Brain Res 221(1):290–294
Anfora G, Frasnelli E, Maccagnani B, Rogers LJ, Vallortigara G (2010) Behavioural and electrophysiological lateralization in a social (Apis mellifera) but not in a non-social (Osmia cornuta) species of bee. Behav Brain Res 206:236–239
Knudsen JT, Tollsten L, Bergström LG (1993) Floral scents-a checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33(2):253–280
Reinhardt J, Sinclair M, Srinivasan MV, Claudianos C (2010) Honeybees learn odour mixtures via a selection of key odorants. PLoS One 5(2):e9110
Laloi D, Bailez O, Blight M, Roger B, Pham-Delegue M-H, Wadhams LJ (2000) Recognition of complex odors by restrained and free-flying honeybees, Apis mellifera. J Chem Ecol 26:2307–2319
Anfora G, Rigosi E, Frasnelli E, Ruga E, Trona F, Vallortigara G (2011) Lateralization in the invertebrate brain: left-right asymmetry of olfaction in bumble bee, Bombus terrestris. PLoS One 6(4):e18903
Frasnelli E, Vallortigara G, Rogers LJ (2011) Right-left antennal asymmetry of odour memory recall in three species of Australian stingless bees. Behav Brain Res 224(1):121–127
Heisenberg M (1994) Central brain function in insects: genetic studies on the mushroom bodies and central complex in Drosophila. Neural basis of behavioural adaptations. Fortschr Zool 39:61–79
Pascual A, Huang K-L, Nevue J, Préat T (2004) Brain asymmetry and long-term memory. Nature 427:605–606
Matsuo R, Kawaguchi E, Yamagishi M, Amano T, Ito E (2010) Unilateral memory storage in the procerebrum of the terrestrial slug Limax. Neurobiol Learn Mem 93:337–342
Kasai Y, Watanabe S, Kirino Y, Matsuo R (2006) The procerebrum is necessary for odor-aversion learning in the terrestrial slug Limax valentianus. Learn Mem 13(4):482–488
Friedrich A, Teyke T (1998) Identification of stimuli and input pathways mediating food-attraction conditioning in the snail, Helix. J Comp Physiol A 183:247–254
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer Science+Business Media LLC
About this protocol
Cite this protocol
Frasnelli, E. (2017). Lateralization in Invertebrates. In: Rogers, L., Vallortigara, G. (eds) Lateralized Brain Functions. Neuromethods, vol 122. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-6725-4_6
Download citation
DOI: https://doi.org/10.1007/978-1-4939-6725-4_6
Published:
Publisher Name: Humana Press, New York, NY
Print ISBN: 978-1-4939-6723-0
Online ISBN: 978-1-4939-6725-4
eBook Packages: Springer Protocols