Asymmetries in mother-infant behaviour in Barbary macaques (Macaca sylvanus)

Introduction

The lateralization in mother-infant interactions has recently been hypothesised to have a perceptual origin in different mammal species, from non-primate mammals (Karenina et al., 2017) to humans (Todd & Banerjee, 2016). In particular, holding infant on the left side of the body has been found to enhance the mother visual and tactile monitoring skill, due to the involvement of the right hemisphere of the brain which is specialised for attention (Whitehead, 1991; Bourne & Todd, 2004; Todd & Banerjee, 2016) and tactile information (Coghill, Gilron & Iadarola, 2001; Sakai et al., 2006). Among mammals the right hemisphere has been found to be more involved in social processing, such as monitoring conspecifics and attending social responses (Rogers, Vallortigara & Andrew, 2013; Quaresmini et al., 2014; Giljov, Karenina & Malashichev, 2018). Moreover, recent studies reported pronounced lateralization of mother-infant behaviour in several non-primate mammals, indicating right-hemisphere dominance for social processing in species of bovids, equids, macropods and marine mammals (Karenina et al., 2017; Giljov, Karenina & Malashichev, 2018). In particular, in all these species infants have been found to prefer keeping the mothers on the left side, compared with the right side, adding further evidence that lateralized mother-infant interactions emerged long before primates (Karenina et al., 2017; Giljov, Karenina & Malashichev, 2018). This left side-right hemisphere preference in the infants has been hypothesised to be advantageous for their survival, favouring mother-infant bonding behaviour and maintenance of spatial proximity (Karenina et al., 2017). Regarding humans, the left-cradling bias found in our species has been hypothesized to be related for example to the infant imprinting to the mother heartbeat, with left-cradling allowing the infant to be close to the mother’s heart (Salk, 1973). Thus, in the presence of an emotional involvement both humans and non-primate mammals seem to choose keeping the conspecifics on their left side. Indeed, the right hemisphere is competent in processing the visuo-spatial information, resulting in an attentional bias toward the left visual hemifield (Karenina et al., 2017). This view has been supported also in other studies of social affiliative behaviour. For example, a left bias for embraces related to positive emotions, a kind of adult cradling, has been reported in humans (Packheiser et al., 2018) and spider monkeys (Boeving, Belnap & Nelson, 2017). According to recent research, the right hemisphere involvement in social stimuli control has also been hypothesized to be a reason for the left-cradling bias reported in the maternal behaviour of humans and some great apes (Hopkins, 2004; Rosa Salva et al., 2012; Giljov, Karenina & Malashichev, 2018). Indeed, research on humans revealed that mothers prefer to cradle their infant on the left side (Salk, 1960; Damerose & Vauclair, 2002) and similar findings have been reported in chimpanzees (Pan troglodytes) (Manning & Chamberlain, 1990; Hopkins et al., 1993; Manning, Heaton & Chamberlain, 1994; E Toback, 1999, unpublished data) and gorillas (Gorilla gorilla) (Manning, Heaton & Chamberlain, 1994) (Table 1). On the other hand, asymmetries in maternal cradling seem to be less clear in Old World monkeys. Indeed, no group-level bias was found for this behaviour in Japanese macaques (Macaca fuscata) (Tanaka, 1989), rhesus macaques (Macaca mulatta) (Tomaszycki et al., 1998), olive baboons (Papio anubis) (Damerose & Hopkins, 2002) and Sichuan snub-nose monkeys (Rhinopithecus roxellana) (Zhao et al., 2008) (Table 1), suggesting phylogenetic differences between taxonomic primate groups. In Old World monkeys, the lack of lateral biases has been found also in other kind of mother-infant interactions, particularly infant retrieval. Indeed, research on rhesus macaques and olive baboons did not report any group-level side preferences in the hand used to retrieve the infant by the mother (Tomaszycki et al., 1998; Damerose & Hopkins, 2002) (Table 1).

Infant nipple preference has been investigated in different non-human primate species, revealing a bias toward the left nipple in wild chimpanzees (Nishida, 1993), captive chimpanzees and bonobos (Pan paniscus) (Hopkins & De Lathouwers, 2006). As reported for maternal cradling, in general no group-level bias in nipple preference has been reported in past research on Old World monkeys, particularly Japanese macaques (Hiraiwa, 1981; Tanaka, 1989), pig-tailed macaques (Macaca nemestrina) (Erwin, Anderson & Bunger, 1975), olive baboons (Damerose & Hopkins, 2002) and Sichuan snub-nose monkeys (Zhao et al., 2008). On the other hand, wild rhesus macaques have been found to show a right nipple preference (Lindburg, 1971) whereas an opposite bias has been reported in a captive group of this species, showing a slight group-level left nipple preference (Tomaszycki et al., 1998). In contrast, more recent research on a large troop of wild rhesus macaques found no group-level nipple preference in this species (Jaffe et al., 2006) (Table 1).

Research on hand preference on different tasks in monkeys and, to a lesser extent, great apes has given rise to a heterogeneous picture of their manual lateralization (for review: Papademetriou, Sheu & Michel, 2005; Fitch & Braccini, 2013). The inconsistency between different studies might be due to methodological differences as well as to the potential influence of factors such as posture (Forsythe et al., 1988; MacNeilage, 2007), task (Fagot & Vauclair, 1991), and individual experience and learning (Westergaard & Suomi, 1993; Hopkins, 1995; Meunier, Blois-Heulin & Vauclair, 2011). One of the main hypotheses aiming to explain patterns of hand preference in primates is the Postural Origin Theory (POT) by MacNeilage (2007). According to the POT, the adoption of terrestrial habits during primate evolution allowed the right hand to become free from postural support duties, getting gradually more involved in tasks requiring specific skill. This process resulted in the pronounced right handedness characterizing humans with their bipedal posture (MacNeilage, 2007; Meguerditchian, Vauclair & Hopkins, 2013; Blois-Heulin et al., 2006). In addition, also the asymmetries in the intrauterine environment as well as in the maternal behaviour and anatomy might play an important role in the development of primate manual lateralization (Previc, 1991; Hepper, Shahidullah & White, 1991; Hopkins, 2004). In fact, basing on previous research, early life asymmetries in mothers and infants have been suggested to be associated with the development of the hand preference of the offspring (Hopkins, 1994; Hopkins, 1995; Westergaard, Byrne & Suomi, 1998; Hopkins, 2004). Moreover, mothers and infant might reciprocally impact their manual lateralization (Scola & Vauclair, 2010). Investigating behavioural asymmetries in mothers and infants might therefore be useful to better understand the development of motor lateralization, particularly handedness in non-human primates, gaining new insight into factors driving the evolution of manual laterality in these species (Hopkins, 2004). However, although literature on humans and chimpanzees is relatively well-represented, more studies are needed involving monkey and prosimian mother-infant dyads (Hopkins, 2004).

The aim of the current study was to verify the presence of behavioural asymmetries in mother-infant dyads in a sample of zoo Barbary macaques (Macaca sylvanus), investigating whether mother lateralization correlates with that of the infant. In particular, for mother macaques we assessed lateralization in maternal cradling and infant retrieval, whereas for the infants we focused on nipple preference and hand use to cling on the mother ventrum. In addition, we tested and investigated the relationship between mother and infant hand preference for food reaching. Basing on previous literature on Old World monkeys, specifically macaques, we expect no bias in maternal cradling and infant retrieval by the mothers (Tomaszycki et al., 1998; Damerose & Hopkins, 2002).

Methods

Results

Maternal cradling and infant retrieval

The median LI (IQR-Interquartile range, minimum, maximum) for maternal cradling was −0.18 (0.91, −0.69, 0.72). At the individual level, six out of seven subjects showed a significant cradling bias, three toward the left hand and three toward the right hand (Table 2). According to a one-sample sign-test, no bias in the distribution of the LI was found (p = 1, N = 7) (Fig. 1). The median LI (IQR, minimum, maximum) for infant retrieval was 0 (0.18, −0.14, 0.22). At the individual level, no macaque showed a significant lateralization (Table 2) and, according to a one-sample sign-test, no bias in the distribution of the LI was found (p = 0.453, N = 7) (Fig. 1).

Table 2:

Measures of lateral biases in mother and infant Barbary macaques.

	Maternal cradling					Infant retrieval
Subject	Right (bouts)	Left (bouts)	Laterality index	z-score	Preference	Right (bouts)	Left (bouts)	Laterality Index	z-score	Preference
Budda	101	34	0.50	5.68	Right	13	11	0.08	0.2	Ambi
Funny	51	77	−0.20	−2.21	Left	11	11	0.00	0	Ambi
Katrina	5	27	−0.69	−3.71	Left	3	4	−0.14	a	a
Last	11	51	−0.65	−4.95	Left	11	7	0.22	0.71	Ambi
Mirror	49	71	−0.18	−1.92	Ambi	18	12	0.20	0.91	Ambi
Vanda	98	16	0.72	7.59	Right	14	14	0.00	0	Ambi
Violetta	74	27	0.47	4.58	Right	24	28	−0.08	−0.42	Ambi

	Infant nipple preference					Clinging on ventrum
	Right (bouts)	Left (bouts)	Laterality index	z-score	Preference	Right (bouts)	Left (bouts)	Laterality Index	z-score	Preference
Budda’s Infant	66	1	0.97	7.82	Right	121	143	−0.08	−1.29	Ambi
Funny’s Infant	63	8	0.77	6.41	Right	122	128	−0.02	−0.32	Ambi
Katrina’s Infant	26	6	0.63	3.36	Right	96	86	0.05	0.67	Ambi
Last’s Infant	69	6	0.84	7.16	Right	122	102	0.09	1.27	Ambi
Mirror’s Infant	32	7	0.64	3.84	Right	143	149	−0.02	−0.29	Ambi
Vanda’s Infant	51	26	0.32	2.74	Right	107	115	−0.04	−0.47	Ambi
Violetta’s Infant	11	46	−0.61	−4.50	Left	159	169	−0.03	−0.5	Ambi

DOI: 10.7717/peerj.4736/table-2

Notes:

aExcluded from the individual-level statistical analysis due to data deficiency.

Ambi: −1.96 < z-score < 1.96; Left: z-score < −1.96; Right: z-score > 1.96.

Lateral biases in mother and infant behaviour

To investigate differences between the lateral biases in the behaviours of the mothers, the LI and ABS-LI for maternal cradling, infant retrieval and food reaching were compared with each other. Pairwise comparisons by Wilcoxon test were corrected for multiplicity with the Bonferroni-Holm method and revealed no significant difference considering both the LI (Fig. 1) and the ABS-LI (Fig. 2) (see Table 3 for W and p values). For infant lateral biases, we compared both the LI and ABS-LI for clinging on mother’s ventrum and food reaching. Wilcoxon test revealed no significant difference when comparing both the LI (W = 13, p = 0.675) (Fig. 1) and the ABS-LI (W = 1, p = 0.059) (Fig. 2). Finally, when considering the relationship between nipple and hand preferences of the infants, a significant correlation was found between the LI for nipple preference and food reaching (rho = 0.786, p = 0.048).

Table 3:

Differences between measures of lateral biases within mother Barbary macaques.

	Cradling	Retrieval	Food reaching
LI
Cradling	#
Retrieval	W = 13.5	#
	p = 1
	p′ = 1
Food reaching	W = 11	W = 13	#
	p = 0.688	p = 0.938
	p′ = 2.064	p′ = 1
ABS-LI
Cradling	#
Retrieval	W = 27	#
	p = 0.031
	p′ = 0.093
Food reaching	W = 23	W = 5	#
	p = 0.150	p = 0.156
	p′ = 0.300	p′ = 0.300

DOI: 10.7717/peerj.4736/table-3

Discussion

Findings from this study highlighted no group-level biases in maternal cradling and infant retrieval by the mothers and the same results emerged for nipple preference and clinging on mother’s ventrum in infants Barbary macaques. Regarding maternal cradling, this study agrees with previous literature on macaques, particularly on rhesus macaques (Tomaszycki et al., 1998) and Japanese macaques (Tanaka, 1989) as well as on other Old-World primates, particularly Sichuan snub-nose monkeys (Zhao et al., 2008). Indeed, no lateral bias in cradling infants has been reported in these species. On the other hand, our results disagree with previous studies reporting a left bias in maternal cradling in great apes, chimpanzees and gorillas (Manning, Heaton & Chamberlain, 1994; E Toback, 1999, unpublished data) and in humans (Salk, 1960; Damerose & Vauclair, 2002), suggesting that consistent behavioural lateralization in mother-infant interactions within the Primates order might have first appeared in hominids. However, at the individual level, four out of seven macaques showed negative LI and z-scores and three of them had a significant left bias. Thus, lateralization in maternal cradling and the possible presence of a left bias in maternal cradling in this species of macaque as well as in other Old-World monkeys deserve further investigation. Regarding the hand preference for infant retrieval by the mother, no group-level bias was reported. This finding is in agreement with previous studies in rhesus macaques (Tomaszycki et al., 1998) and olive baboons (P. anubis) (Damerose & Hopkins, 2002)

In the case of infant nipple use, the finding of a lack of group-level preference is in agreement with previous research on Japanese macaques (Hiraiwa, 1981), pig-tailed macaques (Erwin, Anderson & Bunger, 1975) and wild rhesus macaques (Jaffe et al., 2006), failing to report a group-level bias in using one nipple or the other one. A similar unbiased distribution of nipple preference was found in other Old-World primates, specifically wild Sichuan snub-nose monkeys (Zhao et al., 2008). However, at the individual level six out of seven infant macaques of the current study showed a significant right-nipple preference. Given the small sample size, this high percentage of right biased infants seems to highlight a tendency toward the right nipple. This finding adds consistency to previous research on wild rhesus macaques (Lindburg, 1971) in which a bias toward the right nipple was found. However, the reported right nipple preference is not in agreement with the study on rhesus macaques by Tomaszycki et al. (1998), in which a slight group-level left nipple preference was found. Incongruences between studies might be due to differences in sample size, as the current study has a limited sample, and age of the study subjects. Indeed, the age range of the subjects is smaller in the current study than in the previous one by Tomaszycki et al. (1998) on rhesus macaques. Indeed, our Barbary macaque infants were less than one month old whereas rhesus macaques were observed from birth until they were six weeks old. The individual-level preference for the mother’s right nipple seems partially to resemble the overall tendency to keep the mother on the left side reported in several non-primate species, particularly bovids, cervids, equids, macropods and marine mammals (Karenina et al., 2017; Giljov, Karenina & Malashichev, 2018). However, as infant primates tend to suckle frontally on the mother’s ventrum and nipples are in the middle of the chest, caution is needed before speculating about this result. Further studies on larger samples of animals are needed, considering the potential impact of factors such as age and species on the development of lateral biases in infant primates. Moreover, there might be other possible explanations for the inconsistencies between studies on lateral biases in mothers and infants. For example, it is possible that not all Old-World monkey species share similar mechanism for nipple preference and different housing conditions between studies might also affect the results (Jaffe et al., 2006), as described for other lateralized behaviour (e.g., handedness) (MacNeilage, 2007). As reported for maternal cradling, our findings are in contrast with previous studies on chimpanzees and bonobos (Nishida, 1993; Hopkins & De Lathouwers, 2006), highlighting a left-nipple preference in these species, suggesting differences in lateralization of mother-infant interactions between Old World monkeys and great apes. These findings seem to support the hypothesis relating taxonomic differences in maternal cradling bias and nipple preference to differences in hand preference. In particular, Hopkins (2004) suggested that great apes such as chimpanzees and bonobos showing a left-side bias for cradling and nipple preference tend to have a more pronounced right-hand preference, whereas species with right or no bias in mother-infant interactions tend to be left-handed or ambi-preferent.

In addition, we investigated the hand preference for food reaching in both mother and infant macaques. At the group level, no bias in hand preference was found, either for the mothers nor for the infants. This finding agrees with other studies on Barbary macaques, revealing no group-level hand preference on simple food reaching tasks (Schmitt et al., 2008; Regaiolli, Spiezio & Hopkins, 2018). Moreover, no significant differences were found between mothers and infants in both the LI and the ABS-LI scores, suggesting that mother and infant hand preference is similar in terms of both direction and strength. However, at the individual level, five out of seven mother macaques showed a significant hand preference, whereas no infant was significantly lateralized. This finding seems partially to support the hypothesis that manual lateralization in non-human primates might be affected by the age of the subjects, with older individuals showing a more pronounced hand preference than juveniles (Warren, 1977; Lilak & Phillips, 2008; Meguerditchian, Molesti & Vauclair, 2011). Given the small sample size and the lack of significant differences at the group level, this conclusion is rather speculative and more studies are needed to test the effect of age on the hand preference and to compare manual lateralization between mothers and their infants.

We further investigated differences in the manual lateralization for different behavioural categories involving the use of the hands, considering both direction and strength of the biases. Among the mothers, no significant differences between any measure of lateral bias was found. Similar findings were reported for the infants, showing no significant differences in both the LI and ABS-LI for clinging on mother’s ventrum and food reaching.

In addition, to verify the association between the infants’ suckling bias and their manual lateralization, a correlation with the LI for nipple preference and food reaching was run, revealing a slightly positive correlation between the two behavioural categories. Therefore, the position of the nipple chosen to nurse seems to affect the hand preference to reach for food of the infant. A possible explanation could be that the position of the nipple might affect the hand used to hold on the mother body side. For example, if the infants are suckling on the mother right nipple, which is on the left side with respect to the nursing infants, they could be more comfortable to cling on the mother fur on their left, using the ipsilateral hand. Having a nipple preference might therefore lead to the specific and routine use of one hand for support that may persist also outside the nursing and maternal context. This result seems partially to support the Postural Origin Theory, suggesting a left-hand involvement for posture related activities and the right-hand availability for other tasks (MacNeilage, 2007). Similar influence of infant early bias on hand preference has been reported in capuchin monkeys (Cebus apella). In this species, early bias in head orientation seemed to be related to a body weight displacement of the infant, leading to a manual lateralization for grasping to the mother and to the hand preferences later in development (Westergaard, Byrne & Suomi, 1998). Taken together, our findings seem to underline that the maternal environment and anatomy rather than the mother behaviour and side biases would affect the development of handedness in the infants.

Conclusion

The results of this study showed that at the individual level, infant Barbary macaques showed a distinct nipple preference and similar findings have been found for maternal cradling in mother macaques. However, at the group level, no significant biases were found for any of the behavioural categories considered. This lack of group-level side biases in both the mothers and the infants, specifically for maternal cradling and nipple preference, is not in agreement with previous research on great apes. This discrepancy between studies might be due to taxonomic differences in the infant development and interaction with the mother that might affect the handedness. In other words, the influence of maternal behaviour on the infant lateralization reported in great apes and humans might have appeared late in the phylogeny of primates. However, as suggested by our finding in Barbary macaques, the maternal environment and early choice characterizing the life of the infants might affect their hand preference later in development. The differences in lateral biases in maternal and infant behaviour between monkeys and great apes might also explain incongruences between studies on handedness between the two groups. Indeed, some evidence of population-level right handedness has been frequently reported in great apes (e.g., Meguerditchian et al., 2015; Regaiolli, Spiezio & Hopkins, 2016) but rarely in monkeys, especially during spontaneous unimanual tasks (e.g., Fitch & Braccini, 2013; Regaiolli, Spiezio & Hopkins, 2016). Overall, our study seems to support the hypothesis that maternal environment and anatomy in early life might affect the development of hand preference in non-human primates (Hopkins, 1994; Hopkins, 1995; Westergaard, Byrne & Suomi, 1998; Hopkins, 2004). However, due to the small sample size of the current work and the age differences between different studies, further research on a larger number of mother-infant dyads is needed, in Barbary macaques as well as in other species.

Supplemental Information