Hand preference for a bimanual coordinated task in captive hatinh langurs (Trachypithecus hatinhensis) and grey-shanked douc langurs (Pygathrix cinerea)

Highlights

• We evaluated hand preferences in hatinh and grey-shanked douc langurs for the first time.

• Both species present clear individual lateralisation.

• No group level hand preferences were detected.

• The strength of hand preferences was greater in hatinh than in douc langurs.

• No sex differences were detected within species.

Abstract

Right-handedness in humans reflects the functional brain specialisation of the left hemisphere. To better understand the origins of this population-level tendency, it is crucial to understand manual lateralisation in other non-human primate species. The aim of this article is to present a first approach to the hand preference of two primates from Vietnam, the endangered hatinh langur (Trachypithecus hatinhensis) and the critically endangered grey-shanked douc langur (Pygathrix cinerea). Eighteen individuals from each species (N = 36) were evaluated by means of the bimanual coordinated tube task and their responses were recorded in terms of manual events and bouts. Our results showed that subjects presented strong individual-level preferences but not lateralisation at the group-level. No sex differences were detected within species. The index finger was used in all of the extractions during this bimanual task, alone (86 %) or in combination with other fingers (14 %). In addition, hatinh langurs exhibited a greater strength of hand preferences than grey-shanked douc langurs, pointing to a possible higher manual specialisation during the leaf-eating process. These findings help to broaden our scarce knowledge of manual laterality in Asian colobine monkeys and confirm the bimanual tube task as a sensitive measure for assessing manual laterality in non-human primates.

Introduction

Brain asymmetries in non-human animals have been detected over the last four decades in the brains of fish, amphibians, reptiles and mammals (Bisazza et al., 1998; Braitenberg and Kemali, 1970; Denenberg, 1981; Nottebohm et al., 1976; Rogers et al., 2013; Rogers and Anson, 1979). Nevertheless, it has only recently been accepted that the human brain is not the only lateralised one in the animal kingdom (Corballis, 2020; Miletto Petrazzini et al., 2020; Rogers et al., 2013). Results in this area indicate that there are a significant number of vertebrate species (Hori et al., 2017; Lippolis et al., 2002; Vallortigara et al., 1998; Wiper, 2017), and even some invertebrates (Duistermars et al., 2009; Frasnelli, 2017, 2013; Rogers and Vallortigara, 2019, 2008; Suzuki et al., 2008; Vallortigara and Versace, 2017), that present this characteristic.

Non-human primates have been proposed as a potential model for understanding the evolution and development of human brain asymmetries (Fitch and Braccini, 2013). Some functional asymmetries are particularly suitable to explain human handedness phylogenesis (Cochet and Byrne, 2013). The comparative approach applied to the study of manual laterality helps us understand those processes that led to the strong left-hemisphere brain specialisation observed in modern humans (Hopkins and Cantero, 2003). Socioecological lifestyle, postural characteristics and demands, task-level complexity and tool use have been proposed as factors that could shape the evolution of manual preferences in human and non-human primates (Prieur et al., 2019).

For many years, there has been a strong interest in whether population-level handedness is human-specific or a characteristic also present in non-human animals (Bradshaw and Rogers, 1993; Güntürkün et al., 2020; Rogers and Andrew, 2002). It is now widely accepted that humans are right-handed at the population level, as an estimated 90 % of the population presents this trait (Annett, 2002; Porac and Coren, 1981). Recently, Marcori and Okazaki (2019) reviewed current hypothesis on the origins of human handedness evaluating the effects of genetic, neural asymmetries, pregnancy and socio-cultural influences on human manual laterality. Although most of the reviewed studies did not reject the influence of both genetic and environmental factors, the exact mechanisms responsible for human brain laterality still remain unknown. For this reason, it is believed that a comparative perspective may help unravel the evolution and origins of human cerebral lateralisation (Bradshaw and Rogers, 1993; Hopkins et al., 2015; Llorente et al., 2009; Rogers, 2014; Ward and Hopkins, 1993) and are crucial to understand the functions and pathologies of the asymmetric brain (Güntürkün et al., 2020).

Historically speaking, findings on manual laterality in non-human primates have been inconsistent between and within species (Hopkins, 2006; Papademetriou et al., 2005). Some potential explanations have been proposed to address these issues, including the research setting, statistical approach or task used (Hopkins, 2013a, 2013b). Given that bimanual tasks are cognitively demanding, these tasks are generally more successful in eliciting manual asymmetries than simpler unimanual tasks (Hopkins et al., 2003). These tasks are complex and cognitively demanding, providing more efficiency in detecting manual asymmetries than simple unimanual tasks (Blois-Heulin et al., 2006; Maille et al., 2013). It was Hopkins (1995) who first described the “tube task”, a bimanual coordinated complex device for testing manual preferences in non-human primates. The task involves the provision of a tube containing a preferred food to a primate in order to observe which is the non-dominant hand (used to hold the tube) and which is the dominant hand (used to extract the food from the tube and bring it to the mouth; Hopkins, 1995). According to the task complexity hypothesis (Fagot and Vauclair, 1991), the tube task can be classified as a high-level task, forcing specialised use of the dominant hand to extract the food. Accordingly, the tube task has become a recognised method, which to date has been used to test around 20 different primate species, including cercopithecines (Maille et al., 2013), Rinopithecus roxellana (Zhao et al., 2012), Ateles geoffroyi (Motes Rodrigo et al., 2018), hylobatids (Morino et al., 2017), as well as great apes (Hopkins et al., 2011). Although most tube task experiments have been conducted in captivity (Canteloup et al., 2013; Meunier and Vauclair, 2007; Zhao et al., 2016), some authors have applied this task in wild (Zhao et al., 2012) and semi-wild settings (Llorente et al., 2011). Despite the above, there are still many species which hand preferences have not been investigated. Such investigations could prove helpful in tracing the evolutionary history of primate handedness and the ecological pressures that shape manual use in the primate lineage.

The Asian colobine monkeys or langurs of the Presbytini tribe (Old World monkeys) are medium-sized, generally arboreal monkeys that follow a folivorous diet and whose multi-chambered stomachs have adapted to digest leaves (Brandon-Jones, 2004; Mittermeier et al., 2013; Nadler and Brockman, 2014). Most of the laterality studies conducted on these primates include observations on spontaneous unimanual and bimanual activities during different daily behaviours (Ahamed and Dharmaretnam, 2015; Miller and Paciulli, 2002; Mittra et al., 1997; Pan et al., 2011; Roy and Nagarajan, 2018; Zhao et al., 2010, 2008). For example, 11 red-shanked douc langurs (Pygathrix nemaeus) at the Cologne Zoo were evaluated for hand function based on the degree of fine motor skills required for the behaviours observed. The results yielded four individuals with right-hand preferences and four with left-hand preferences, leading the authors to conclude an absence of population-level handedness (Smith and Scollay, 2001). Zhao et al. (2012) performed a study using the tube task on wild Sichuan snub-nosed monkeys (Rhinopithecus roxellana) and found tentative evidence of group-level left-handedness in this species of Cercopithecoidea. Our study constitutes a first approach to measuring manual laterality among hatinh langurs (Trachypithecus hatinhensis) and grey-shanked douc langurs (Pygathrix cinerea) using the coordinated bimanual tube task. Our main objectives were to: (1) determine whether these langurs present individual hand preferences and/or group level handedness, (2) assess whether sexes or species differed in the strength and/or direction of hand preferences, and (3) evaluate finger use on food extraction. Based on previous reports we predicted that langurs would present clear individual hand preferences but fail to show group-level handedness (Miller and Paciulli, 2002; Zhao et al., 2016), that no sex or species differences would be detected (Fu et al., 2019; Zhao et al., 2007), and finally, that the index finger would be the one most recurrently used in this bimanual task (Maille et al., 2013; Zhao et al., 2012).