Forelimb preferences in quadrupedal marsupials and their implications for laterality evolution in mammals

BMC Evolutionary Biology

Yegor Malashichev²  Karina Karenina¹  Andrey Giljov¹ 

[1] Department of Vertebrate Zoology, Saint Petersburg State University, Saint Petersburg, Russia;Department of Embryology, Saint Petersburg State University, St. Petersburg, Russia

关键词: Quadruped;    Postural effect;    Sex effect;    Sugar glider;    Grey short-tailed opossum;    Marsupial;    Hand preference;    Forelimb preference;    Lateralization;   

Others  :  1129580
DOI  :  10.1186/1471-2148-13-61

 received in 2012-04-05, accepted in 2013-01-15,  发布年份 2013

【 摘 要 】

Background

Acquisition of upright posture in evolution has been argued to facilitate manual laterality in primates. Owing to the high variety of postural habits marsupials can serve as a suitable model to test whether the species-typical body posture shapes forelimb preferences in non-primates or this phenomenon emerged only in the course of primate evolution. In the present study we aimed to explore manual laterality in marsupial quadrupeds and compare them with the results in the previously studied bipedal species. Forelimb preferences were assessed in captive grey short-tailed opossum (Monodelphis domestica) and sugar glider (Petaurus breviceps) in four different types of unimanual behaviour per species, which was not artificially evoked. We examined the possible effects of sex, age and task, because these factors have been reported to affect motor laterality in placental mammals.

Results

In both species the direction of forelimb preferences was strongly sex-related. Male grey short-tailed opossums showed right-forelimb preference in most of the observed unimanual behaviours, while male sugar gliders displayed only a slight, not significant rightward tendency. In contrast, females in both species exhibited consistent group-level preference of the left forelimb. We failed to reveal significant differences in manual preferences between tasks of potentially differing complexity: reaching a stable food item and catching live insects, as well as between the body support and food manipulation. No influence of subjects’ age on limb preferences was found.

Conclusions

The direction of sex-related differences in the manual preferences found in quadrupedal marsupials seems to be not typical for placental mammals. We suggest that the alternative way of interhemispheric connection in absence of corpus callosum may result in a fundamentally distinct mechanism of sex effect on limb preferences in marsupials compared to placentals. Our data confirm the idea that non-primate mammals differ from primates in sensitivity to task complexity. Comparison of marsupial species studied to date indicate that the vertical body orientation and the bipedalism favor the expression of individual– and population–level forelimb preferences in marsupials much like it does in primates. Our findings give the first evidence for the effect of species-typical posture on the manual laterality in non-primate mammals.

【 授权许可】

   
2013 Giljov et al; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Rogers LJ, Workman L: Footedness in birds. Anim Behav 1993, 45:409-411.
• [2]Bisazza A, Lippolis G, Vallortigara G: Lateralization of ventral fins use during object exploration in the blue gourami (Trichogaster trichopterus). Physiol Behav 2001, 72:575-578.
• [3]Hook MA: The evolution of lateralized motor functions. In Comparative Vertebrate Cognition. Edited by Rogers LJ, Kaplan G. New York: Kluwer; 2004:325-370.
• [4]Malashichev YB: One-sided limb preference is linked to alternating-limb locomotion in anuran amphibians. J Comp Psychol 2006, 120:401-410.
• [5]Stancher G, Clara E, Regolin L, Vallortigara G: Lateralized righting behaviour in the tortoise (Testudo hermanni). Behav Brain Res 2006, 173:315-319.
• [6]MacNeilage PF, Rogers LJ, Vallortigara G: Origins of the left and right brain. Sci. Amer. 2009, 301:60-67.
• [7]Annett M: Handedness and Brain Asymmetry: the Right Shift Theory. Hove: Psychology Press; 2002.
• [8]Ward JP: Laterality in African and Malagasy prosimians. In Creatures of the Dark: the Nocturnal Prosimians. Edited by Altermann L, Doyle GA, Izard MK. New York: Plenum Press; 1995:293-309.
• [9]Hopkins WD: Comparative and familial analysis of handedness in great apes. Psychol Bull 2006, 132:538-559.
• [10]Clark MM, Robertson RK, Galef BG: Intrauterine position effects on sexually dimorphic asymmetries of Mongolian gerbils: testosterone, eye opening, and paw preference. Dev Psychobiol 1993, 26:185-194.
• [11]Collins RL: On the inheritance of direction and degree of asymmetry. In Cerebral Lateralization in Nonhuman Species. Edited by Glick SD. Orlando, FL: Academic; 1985:41-71.
• [12]Betancur C, Neveu PJ, Le Moal M: Strain and sex differences in the degree of paw preference in mice. Behav Brain Res 1991, 45:97-101.
• [13]Biddle FG, Coffaro CM, Ziehr JE, Eales BA: Genetic variation in paw preference (handedness) in the mouse. Genome 1993, 36:935-943.
• [14]Güven M, Elalmis DD, Binokay S, Tan U: Population-level right-paw preference in rats assessed by a new computerized food-reaching test. Int J Neurosci 2003, 113(12):1675-1689.
• [15]Reimchen TE, Spoljaric MA: Right paw foraging bias in wild black bear (Ursus americanus kermodei). Laterality 2011, 16:471-478.
• [16]Tan Ü, Yaprak M, Kutlu N: Paw preference in cats: Distribution and sex differences. Int J Neurosci 1990, 50:195-208.
• [17]Tan Ü, Kutlu N: The distribution of paw preference in right-, left-, and mixed pawed male and female cats: The role of a female right-shift factor in handedness. Int J Neurosci 1991, 59:219-229.
• [18]Fabre-Thorpe M, Fagot J, Lorincz E, Levesque F, Vauclair J: Laterality in cats: paw preference and performance in a visuomotor activity. Cortex 1993, 29:15-24.
• [19]Pike AVL, Maitland DP: Paw preferences in cats (Felis silvestris catus) living in a household environment. Behav Proc 1997, 39:241-247.
• [20]Wells DL, Millsopp S: Lateralized behaviour in the domestic cat, Felis silvestris catus. Anim Behav 2009, 78:537-541.
• [21]Tan Ü: Paw preferences in dogs. Int J Neurosci 1987, 32:825-829.
• [22]Wells DL: Lateralised behaviour in the domestic dog, Canis familiaris. Behav Proc 2003, 61:27-35.
• [23]Quaranta A, Siniscalchi M, Frate A, Vallortigara G: Paw preference in dogs: relations between lateralised behaviour and immunity. Behav Brain Res 2004, 153:521-525.
• [24]Hackert R, Maes LD, Herbin M, Libourel PA, Abourachid A: Limb preference in the gallop of dogs and the half-bound of pikas on flat ground. Laterality 2008, 13:310-319.
• [25]Austin NP, Rogers LJ: Limb preferences and lateralization of aggression, reactivity and vigilance in feral horses, Equus caballus. Anim Behav 2012, 83:239-247.
• [26]Murphy J, Sutherland A, Arkins S: Idiosyncratic motor laterality in the horse. Appl Anim Behav Sci 2005, 91:297-310.
• [27]McGreevy PD, Thomson PC: Differences in motor laterality between breeds of performance horse. Appl Anim Behav Sci 2006, 99:183-190.
• [28]Williams DE, Norris BJ: Laterality in stride pattern preferences in racehorses. Anim Behav 2007, 74:941-950.
• [29]McGreevy PD, Landrieu JP, Malou PFJ: A note on motor laterality in plains zebras (Equus burchellii) and impalas (Aepyceros melampus). Laterality 2007, 12:449-457.
• [30]Zucca P, Cerri F, Carluccio A, Baciadonna L: Space availability influence laterality in donkeys (Equus asinus). Behav Proc 2011, 88:63-66.
• [31]Zucca P, Palladini A, Baciadonna L, Scaravelli D: Handedness in the echolocating Schreiber’s long-fingered bat (Miniopterus schreibersii). Behav Proc 2010, 84(3):693-695.
• [32]Levermann N, Galatius A, Ehlme G, Rysgaard S, Born EW: Feeding behaviour of free-ranging walruses with notes on apparent dextrality of flipper use. BMC Ecol 2003, 3:9. BioMed Central Full Text
• [33]Clapham PJ, Leimkuhler E, Gray BK: Do humpback whales exhibit lateralized behaviour? Anim Behav 1995, 50:73-82.
• [34]Sakai M, Hishii T, Takeda S, Kohshima S: Laterality of flipper rubbing behaviour in wild bottlenose dolphins (Tursiops aduncus): Caused by asymmetry of eye use? Behav Brain Res 2006, 170:204-210.
• [35]Gómez-Campos E, Aguilar A, Goodall RN: Serrated flippers and directional asymmetry in the appendicular skeleton of the Commerson’s dolphin (Cephalorhynchus commersonii). Anat Rec 2010, 293:1816-1824.
• [36]Rogers LJ: Hand and paw preferences in relation to the lateralized brain. Phil Trans R Soc B 2009, 364:943-954.
• [37]Westergaard GC, Kuhn HE, Suomi SJ: Bipedal posture and hand preference in humans and other primates. J Comp Psychol 1998, 112:56-63.
• [38]Braccini S, Lambeth S, Schapiro S, Fitch WT: Bipedal tool use strengthens chimpanzee hand preferences. J Hum Evol 2010, 58(3):234-241.
• [39]Scheumann M, Joly-Radko M, Leliveld L, Zimmermann E: Does body posture influence hand preference in an ancestral primate model? BMC Evol Biol 2011, 11:52. BioMed Central Full Text
• [40]Ward JP, Milliken GW, Stafford DK: Patterns of lateralized behavior in prosimians. In Primate Laterality: Current Behavioral Evidence of Primate Asymmetries. Edited by Ward JP, Hopkins WD. New York: Springer; 1993:43-76.
• [41]Leliveld LMC, Scheumann M, Zimmermann E: Manual lateralization in early primates: A comparison of two mouse lemur species. Am J Phys Anthropol 2008, 137(2):156-163.
• [42]Olson DA, Ellis JE, Nadler RD: Hand preferences in captive gorillas, orangutans and gibbons. Am J Primatol 1990, 20:83-94.
• [43]Perelle IB, Ehrman L: An international study of human handedness: the data. Behav Genet 1994, 24:217-227.
• [44]Corbetta D: Right-handedness may have come first: Evidence from studies in human infants and nonhuman primates. Behav Brain Sci 2003, 26:217-218.
• [45]Giljov A, Karenina K, Malashichev Y: Limb preferences in a marsupial, Macropus rufogriseus: evidence for postural effect. Anim Behav 2012, 83(2):525-534.
• [46]Ward JP, Milliken GW, Dodson DL, Stafford DK, Wallace M: Handedness as a function of sex and age in a large population of Lemur. J Comp Psychol 1990, 104:167-173.
• [47]Spinozzi G, Truppa V: Hand preference in different tasks by tufted capuchins (Cebus apella). Int J Primatol 1999, 20:827-848.
• [48]Corp N, Byrne RW: Sex difference in chimpanzee handedness. Am J Phys Anthropol 2004, 123:62-68.
• [49]Milliken GW, Ferra G, Kraiter KS, Ross CL: Reach and posture hand preferences during arboreal feeding in sifakas (Propithecus sp.): a test of the postural origins theory of behavioral lateralization. J Comp Psychol 2005, 119:430-439.
• [50]Bennett AJ, Suomi SJ, Hopkins WD: Effects of early adverse experiences on behavioural lateralisation in rhesus monkeys (Macaca mulatta). Laterality 2008, 13:282-292.
• [51]Humle T, Matsuzawa T: Laterality in hand use across four tool use behaviors among the wild chimpanzees of Bossou, Guinea. West Africa. Am J Primatol 2009, 71:40-48.
• [52]Sommer IE, Aleman A, Somers M, Boks MP, Kahn RS: Sex differences in handedness, asymmetry of the Planum Temporale and functional language lateralization. Brain Res 2008, 1206:76-88.
• [53]Pan J, Xiao W, Zhao Q: Hand preference by black-and-white snub-nosed monkeys (Rhinopithecus bieti) in captivity: Influence of tasks and sexes. Laterality 2011, 16:656-672.
• [54]Lehman RAW: Distribution and changes in strength of hand preference of Cynomolgus monkeys. Brain Behav Evol 1980, 17:209-217.
• [55]Vauclair J, Fagot J: Spontaneous hand usage and handedness in a troop of baboons. Cortex 1987, 23:265-274.
• [56]King JE: Laterality in hand preference and reaching accuracy of cotton-top tamarins (Saguinus oedipus). J Comp Psychol 1995, 109:34-41.
• [57]Harrison KH, Byrne R: Hand preferences in unimanual and bimanual feeding by wild vervet monkeys (Cercopithecus aethiops). J Comp Psychol 2000, 114:13-21.
• [58]Vauclair J, Meguerditchian A, Hopkins WD: Hand preferences for unimanual and coordinated bimanual tasks in baboons (Papio anubis). Cogn Brain Res 2005, 25:210-216.
• [59]Meunier H, Vauclair J: Hand preferences on unimanual and bimanual tasks in white-faced capuchins (Cebus capucinus). Am J Primatol 2007, 69:1064-1069.
• [60]Lhota S, Jůunek T, Bartoš L: Patterns and laterality of hand use in free-ranging aye-ayes (Daubentonia madagascariensis) and a comparison with captive studies. J Ethol 2009, 27:419-428.
• [61]McGreevy PD, Brueckner A, Thomson PC, Branson NJ: Motor laterality in 4 breeds of dog. J Vet Behav 2010, 5:318-323.
• [62]Byrne RW, Byrne JM: Hand preferences in the skilled gathering tasks of mountain gorillas (Gorilla g. berengei). Cortex 1991, 27:521-546.
• [63]Hopkins WD: Posture and reaching in chimpanzees (Pan troglodytes) and orangutans (Pongo pygmaeus). J Comp Psychol 1993, 17:162-168.
• [64]Meguerditchian A, Calcutt SE, Lonsdorf EV, Ross SR, Hopkins WD: Captive gorillas are right-handed for bimanual feeding. Am J Phys Anthropol 2010, 141:638-645.
• [65]Milliken GW, Stafford DK, Dodson DL, Pinger CD, Ward JP: Analyses of feeding lateralization in the small-eared bush baby (Otolemur garnettii): a comparison with the ring-tailed lemur (Lemur catta). J Comp Psychol 1991, 105:274-285.
• [66]Sugiyama Y, Fushimi T, Sakura O, Matsuzawa T: Hand preference and tool use in wild chimpanzees. Primates 1993, 34:151-159.
• [67]Westergaard GC, Suomi SJ: Hand preference in capuchin monkeys varies with age. Primates 1993, 34:295-299.
• [68]Westergaard GC, Suomi SJ: The use of probing tools by capuchin monkeys: evidence of increases right hand use with age. Int J Primatol 1994, 15:521-529.
• [69]Hopkins WD, Fernández-Carriba S: The effect of situational factors on hand preferences for feeding in 177 captive chimpanzees (Pan troglodytes). Neuropsychologia 2000, 38(4):403-409.
• [70]Boesch C: Handedness in wild chimpanzees. Int J Primatol 1991, 6:541-558.
• [71]Laska M: A study of correlates of hand preferences in squirrel monkeys (Saimiri sciureus). Primates 1996, 37:457-465.
• [72]Kalisch T, Wilimzig C, Kleibel N, Tegenthoff M, Dinse HR: Age-related attenuation of dominant hand superiority. PLoS One 2006, 1(1):e90.
• [73]Fagot J, Vauclair J: Manual laterality in nonhuman primates: a distinction between handedness and manual specialization. Psychol Bull 1991, 109:76-89.
• [74]Blois-Heulin C, Guitton JS, Nedellec-Bienvenue D, Ropars L, Vallet E: Hand preference in unimanual and bimanual tasks and postural effect on manual laterality in captive red-capped mangabeys (Cercocebus torquatus torquatus). Am J Primatol 2006, 68:429-444.
• [75]Chapelain A, Bec P, Blois-Heulin C: Manual laterality in Campbell’s monkeys (Cercopithecus c. campbelli) in spontaneous and experimental actions. Behav Brain Res 2006, 173:237-245.
• [76]Schweitzer C, Bec P, Blois-Heulin C: Does the complexity of the task influence manual laterality in De Brazza’s monkeys (Cercopithecus neglectus)? Ethology 2007, 113:983-994.
• [77]Lilak AL, Phillips KA: Consistency of hand preference across low-level and high-level tasks in capuchin monkeys (Cebus apella). Am J Primatol 2008, 70:254-260.
• [78]King JE, Landau VI: Manual preference in varieties of reaching in squirrel monkeys. In Primate Laterality: Current Behavioral Evidence of Primate Asymmetries. Edited by Ward JP, Hopkins WD. New York: Springer; 1993:107-124.
• [79]Lippolis G, Westman W, McAllan BM, Rogers LJ: Lateralisation of escape responses in the stripe-faced dunnart Sminthopsis macroura (Dasyuridae: Marsupialia). Laterality 2005, 10:457-470.
• [80]Descovich KA, Reints Bok TE, Lisle AT, Phillips CJC: Auditory laterality in a nocturnal, fossorial marsupial (Lasiorhinus latifrons) in response to bilateral stimuli. Lateralityin press
• [81]Megirian D, Weller L, Martin GF, Watson CRR: Aspects of laterality in the marsupial Trichosurus vulpecula (brush-tailed possum). Ann NY Acad Sci 1977, 299:197-212.
• [82]Ivanco TL, Pellis SM, Whishaw IQ: Skilled forelimb movements in prey catching and in reaching by rats (Rattus norvegicus) and opossums (Monodelphis domestica): relations to anatomical differences in motor systems. Behav Brain Res 1996, 79:163-181.
• [83]Luo ZX, Ji Q, Wible JR, Yuan CX: An early Cretaceous tribosphenic mammal and metatherian evolution. Science 2003, 302:1934-1940.
• [84]Karlen SJ, Krubitzer LA: The functional and anatomical organization of marsupial neocortex: evidence for parallel evolution across mammals. Prog Neurobiol 2007, 82:122-141.
• [85]Konerding WS, Hedrich HJ, Bleich E, Zimmermann E: Paw preference is not affected by postural demand in a nonprimate mammal (Felis silvestris catus). J Comp Psychol 2012, 126:15-22.
• [86]Armati PJ, Dickman CR, Hume ID: Marsupials. Cambridge: Cambridge University Press; 2006.
• [87]Webster KN, Dawson TJ: Locomotion energetics and gait characteristics of a rat-kangaroo, Bettongia penicillata, have some kangaroo-like features. J Comp Physiol B Biochem Syst Environ Physiol 2003, 173:549-557.
• [88]Ribeiro-Carvalho A, Abreu-Villaça Y, Paes-Branco D, Filgueiras CC, Manhães AC: Novelty affects paw preference performance in adult mice. Anim Behav 2010, 80:51-57.
• [89]Zucca P, Baciadonna L, Masci S, Mariscoli M: Illness as a source of variation of laterality in lions (Panthera leo). Laterality 2011, 16:356-366.
• [90]Rogers LJ: Relevance of brain and behavioural lateralization to animal welfare. Appl Anim Behav Sci 2010, 127:1-11.
• [91]Stafford DK, Milliken GW, Ward JP: Lateral bias in feeding and brachiation in Hylobates. Primates 1990, 31:407-414.
• [92]Spinozzi G, Truppa V: Problem-solving srategies and hand preferences for a multicomponent task by tufted capuchins (Cebus apella). Int J Primatol 2002, 23(3):621-638.
• [93]Wells DL, Millsopp S: The ontogenesis of lateralized behavior in the domestic cat, Felis silvestris catus. J Comp Psychol 2012, 126(1):23-30.
• [94]Geschwind N, Galaburda AM: Cerebral lateralization: biological mechanisms, associations, and pathology. Cambridge, MA: MIT Press; 1987.
• [95]Heath CJ, Jones EG: Interhemispheric pathways in the absence of a corpus callosum: An experimental study of commissural connexions in the marsupial phalanger. J Anat 1971, 109:253-270.
• [96]Hopkins WD, Rilling JK: A comparative MRI study of the relationship between neuroanatomical asymmetry and interhemispheric connectivity in primates: Implication for the evolution of functional asymmetries. Behav Neurosci 2000, 114:739-748.
• [97]Bloom JS, Hynd GW: The role of the corpus callosum in interhemispheric transfer of information: excitation or inhibition? Neuropsychol Rev 2005, 15:59-71.
• [98]Hopkins WD, Dunham L, Cantalupo C, Taglialatela JP: The association between handedness, brain asymmetries, and corpus callosum size in chimpanzees (Pan troglodytes). Cereb Cortex 2007, 17:1757-1765.
• [99]de Lacoste MC, Woodward DJ: The corpus calosum in nonhuman primates: Determinants of size. Brain Behav Evol 1988, 31:318-323.
• [100]Witelson SF, Goldsmith CH: The relationship of hand preference to anatomy of the corpus callosum in men. Brain Res 1991, 545:175-182.
• [101]Phillips KA, Sherwood CC, Lilak AL: Corpus callosum morphology in capuchin monkeys is influenced by sex and handedness. PLoS One 2007, 2(8):e792.
• [102]Hellner-Burris K, Sobieski CA, Gilbert VR, Phillips KA: Prey capture efficiency in brown capuchin monkeys (Cebus apella) is influenced by sex and corpus callosum morphology. Am J Primatol 2010, 72(6):502-508.
• [103]Fadem BH, Kraus DB, Sheffet RH: Nest-building in gray short-tailed opossums: Temperature effects and sex differences. Physiol Behav 1986, 36:667-670.
• [104]Kondratyeva L, Ilchenko O: Behaviour of sugar glider (Petaurus breviceps) in Moscow zoo. I. Elements of behaviour. In Scientific Research in Zoological Parks. Volume 22. Edited by Spicin VV, Popov SV, Vahrusheva GV. Moscow: Moscow Zoo; 2007:88-113.
• [105]Manning JT: Sex differences in left-side infant holding: results from “family album” photographs. Ethol Sociobiol 1991, 12:337-343.
• [106]Damerose E, Vauclair J: Posture and laterality in human and non-human primates: Asymmetries in maternal handling and infant’s early motor asymmetries. In Comparative Vertebrate Lateralization. Edited by Rogers LJ, Andrew RJ. Oxford: Oxford University Press; 2002:306-362.
• [107]Cameron R, Rogers LJ: Hand preference of the common marmoset (Callithrix jacchus): problem solving and responses in a novel setting. J Comp Psychol 1999, 113:149-157.
• [108]MacNeilage PF, Studdert-Kennedy MG, Lindblom B: Primate handedness reconsidered. Behav Brain Sci 1987, 10:247-303.
• [109]MacNeilage PF: The ‘postural origins’ theory of primate neurobiological asymmetries. In Biological and Behavioral Determinants of Language Development. Edited by Krasnegor NA, Rumbaugh DM, Schiefelbusch RL, Studdert-Kennedy MG. Hillsdale, New Jersey: L. Erlbaum; 1991:165-188.
• [110]MacNeilage PF: Present status of the postural origins theory. In The Evolution of Hemispheric Specialization in Primates. Edited by Hopkins WD. Oxford: Elsevier; 2007:59-91.
• [111]Rigamonti MM, Spiezio C, Poli MD, Fazio F: Laterality of manual function in foraging and positional behavior in wild indri (Indri indri). Am J Primatol 2005, 65:27-38.
• [112]Hopkins WD: Brief communication: Locomotor limb preferences in captive chimpanzees (Pan troglodytes): implications for morphological asymmetries in limb bones. Am J Phys Anthropol 2008, 137:113-118.
• [113]Pridmore PA: Trunk movements during locomotion in the marsupial Monodelphis domestica (Didelphidae). J Morphol 1992, 211:137-146.
• [114]Nowak RM: Walker’s Mammals of the World. Volume 2. 6th edition. Baltimore: The Johns Hopkins University Press; 1999.
• [115]Shapiro LJ, Young JW: Is primate-like quadrupedalism necessary for fine-branch locomotion? A test using sugar gliders (Petaurus breviceps). J Hum Evol 2010, 58(4):309-319.
• [116]Hopkins WD, Bennett A, Bales SL, Lee J, Ward JP: Behavioral laterality in captive bonobos (Pan paniscus). J Comp Psychol 1993, 107:403-410.
• [117]Blois-Heulin C, Bernard V, Bec P: Postural effect on manual laterality in different tasks in captive grey-cheeked mangabey (Lophocebus albigena). J Comp Psychol 2007, 121:205-213.
• [118]Dodson DL, Stafford D, Forsythe C, Seltzer CP, Ward JP: Laterality in quadrupedal and bipedal prosimians: reach and whole-body turn in the mouse lemur (Microcebus murinus) and the galago (Galago moholi). Am J Primatol 1992, 26:191-202.
• [119]McGrew WC, Marchant LF: On the other hand: Current issues in and meta-analysis of the behavioral laterality of hand function in nonhuman primates. Yearbook Phys Anthropol 1997, 40:201-232.
• [120]Eisenberg J, Redford K: Mammals of the Neotropics: The Central Neotropics. Chicago, IL: The University of Chicago Press; 1999. 3
• [121]Jackson SM: Australian mammals: biology and captive management. Melbourne: CSIRO Publishing; 2003.
• [122]Unger K: Nest-building behavior of the Brazilian bare-tailed opossum, Monodelphis domestica. J Mammal 1982, 63(1):160-162.
• [123]Tomkins LM, McGreevy PD, Branson NJ: Lack of standardization in reporting motor laterality in the domestic dog (Canis familiaris). J Vet Behav 2010, 5:235-239.
• [124]MacNeilage PF: Implications of primate functional asymmetries for the evolution of cerebral hemispheric specializations. In Primate Laterality: Current Behavioral Evidence of Primate Asymmetries. Edited by Ward JP, Hopkins WD. New York: Springer; 1993:319-341.
• [125]Papademetriou E, Sheu CF, Michel GF: A meta-analysis of primate hand preferences, particularly for reaching. J Comp Psychol 2005, 119:33-48.