Precise digit use increases the expression of handedness in Colombian spider monkeys (Ateles fusciceps rufiventris)

Abstract

Decades of research on the hand use patterns of nonhuman primates can be aptly summarized by the following phrase: measurement matters. There is a general consensus that simple reaching is a poor indicator of handedness in most species, while tasks that constrain how the hands are used elicit individual, and in some cases, population-level biases. The TUBE task has become a popular measure of handedness, although there is variability in its administration across studies. The goal of this study was to investigate whether TUBE performance is affected by tube diameter, with the hypothesis that decreasing tube diameter would increase task complexity, and therefore the expression of handedness. We predicted that hand preference strength, but not direction, would be affected by tube diameter. We administered the TUBE task using a 1.3 cm tube to Colombian spider monkeys, and compared their performance to a previous study using a larger 2.5 cm diameter tube. Hand preference strength increased significantly on the smaller diameter tube. Hand preference direction was not affected. Notably, spider monkeys performed the TUBE task using a single digit, despite the longstanding view that this species has poor dexterity. We encourage investigators who use the TUBE task to carefully consider the diameter of the tube used in testing, and to report digit use consistently across studies. In addition, we recommend that researchers who cannot use the TUBE task try to incorporate the key features from this task into their own species appropriate measures: bimanual coordination and precise digit use.

Handedness for Unimanual Grasping in 564 Great Apes: The Effect on Grip Morphology and a Comparison with Hand Use for a Bimanual Coordinated Task

“…We further showed in this study that grasping morphology when reaching for a small food item differed between species and hands and that only TI grips elicited a predominance of right-handedness. Moreover, similar effect of fine precision grip on the degree of right-handedness has been found in young human infants for bimanual tasks ( Potier et al, 2013 ), indicating that grip morphology including to use of single digit in precision movements is an important factor in the expression of individual hand preferences ( Maille et al, 2013 ; Nelson and Boeving, 2015 ). Consistent with some previous reports ( Christel, 1994 ; Christel et al, 1998 ; Pouydebat et al, 2011 ), gorillas and bonobos showed the highest percentages in thumb-index grasping responses compared to chimpanzees and orangutans.…”

Hand preferences in two unimanual and two bimanual coordinated tasks in the black-handed spider monkey (Ateles geoffroyi).

“…Nevertheless, a recent study found that Colombian spider monkeys ( Ateles fusciceps rufiventris ) are clearly able to perform the tube task and that they display significant hand preferences at the individual, but not at the population, level in this task (Nelson, Figueroa, Albright, & Gonzalez, 2015). A follow-up study confirmed this finding and further reported that the inner diameter of the tube systematically affected the strength, but not the direction of hand preference, which is consistent with the notion that task complexity or the degree of fine motor skills required correlates positively with the expression of hand preference (Nelson & Boeving, 2015).…”

“…This notion is supported by our finding that, with only few exceptions, all AbsHI scores in the three tube tasks were ≥0.80 (Tables 1– 3), leaving only little room for between-task differences. Second, the effects of presence or absence of postural support (in the unimanual vs. bimanual tube tasks) and of the difference in motor precision required (in the big vs. small tube task) that have been reported in other studies (Canteloup et al, 2013; Nelson & Boeving, 2015) may not have been big enough for the spider monkeys to have a significant impact on the strength of hand preference. In this context, it should also be mentioned that success rate, another measure of task demand, was 100% in all three tube tasks, meaning that the spider monkeys always succeeded in retrieving the food from the tubes.…”

“…Our finding that black-handed spider monkeys display significant hand preferences at the individual, but not at the population, level is in line with the majority of studies that used the tube task with other species (e.g., rhesus macaques: Bennett et al, 2008; Tonkean macaques: Canteloup et al, 2013; capuchin monkeys: Lilak & Phillips, 2008; squirrel monkeys: Meguerditchian et al, 2012; De Brazza’s monkeys and red-capped mangabeys: Maille et al, 2013). Another member of the genus Ateles , that is, the Colombian spider monkey ( A. fusciceps rufiventris ), has also been found to only display significant hand preferences at the individual level in this bimanual coordination task (Nelson & Boeving, 2015). Studies that reported population-level hand preferences in the tube task are so far mainly restricted to the Great Apes (chimpanzees, bonobos, gorillas, and orangutans: Hopkins et al, 2011) and the Lesser Apes (siamangs and white-cheeked gibbons: Morino et al, 2017).…”

Lateralization and performance asymmetries in the termite fishing of wild chimpanzees in the goualougo triangle, republic of Congo

“…For instance, 10 nonhuman primates species have been tested on a measure of coordinated bimanual actions referred to as the tube task [Hopkins et al, ; Meguerditchian et al, ]. When the data are summed across all studies, gorillas, chimpanzees, and baboons show population‐level right handedness whereas orangutans, red‐capped mangabeys, snub nose monkeys, and spider monkeys show a significant left hand bias [Hopkins et al, ; Maille et al, ; Nelson & Boeving, ; Nelson et al, ; Schweitzer et al, ; Vauclair et al, ; Zhao et al, ]. Bonobos, capuchin, squirrel, rhesus, and barbary macaque monkeys fail to show a population‐level bias [Bennett et al, ; Chapelain et al, ; Meguerditchian et al, ; Meunier & Vauclair, ; Schmitt et al, ; Spinozzi et al, ].…”