Correction: Division of Labor in Hand Usage Is Associated with Higher Hand Performance in Free-Ranging Bonnet Macaques, Macaca radiata

This article was republished on April 8, 2015, to correct an error in the title and abstract that was introduced during the production process: "Macaca radiata" was changed to "Macaca radiate.” The publisher apologizes for the error. Please download this article again to view the correct version. The originally published, uncorrected article and the republished, corrected article are provided here for reference.

hitting an opponent) and those requiring physical strength (e.g., climbing), as 23 described by Mangalam et al. [1], is associated with higher hand performance in 24 free-ranging bonnet macaques, Macaca radiata. We determined the extent to 25 which (a) the macaques exhibit laterality in hand usage in an experimental unimanual and a bimanual food-reaching task, and (b) manual laterality is 27 associated with hand performance in an experimental hand-performance-28 differentiation task. We found strong negative relationships between (a) the 29 performance of the preferred hand in the hand-performance-differentiation task 30 (measured as the latency in food extraction; lower latency = higher 31 performance), the preferred hand determined using the bimanual food-reaching 32 captive gorillas, Gorilla gorilla [19] and chimpanzees [20] preferentially used one 79 hand to take the food items towards the mouth, and the other hand to hold the 80 remaining ones. While extracting peanuts from a lidded box captive tufted 81 capuchin monkeys consistently used one hand to open the lid of the box and the 82 other hand to reach for them [21]. While allogrooming, wild Sichuan snub-nosed 83 monkeys [22] and both captive and wild chimpanzees [23] preferentially used 84 one hand to hold the skin, and the other hand to remove dirt and ectoparasites. 85 Mangalam et al. [1] argued that these observations might reflect specialization 86 of the two hands for manual actions requiring different dexterity types (i.e., 87 simple/complex hand movements in three-dimensional space, grasping, 88 supporting the body, etc.), and along similar lines described division of labor in 89 hand usage in free-ranging bonnet macaques, Macaca radiata. The macaques 90 preferentially used the 'preferred' hand for manual actions requiring 91 maneuvering in three-dimensional space (reaching for food, grooming, and 92 hitting an opponent), and the 'nonpreferred' hand for those requiring physical 93 strength (climbing). In a hand-performance-differentiation task that 94 ergonomically forced the usage of one particular hand, the macaques extracted 95 food faster with the maneuvering hand compared to the supporting hand, 96 demonstrating the higher maneuvering dexterity of the maneuvering hand. 97 However, whether such division of labor in hand usage improves hand 98 performance in terms of the time and/or energy required to solve a given task 99 remains unexplored. 100

101
In the present study, we examined whether the division of labor in hand usage, 102 as described by Mangalam et al. [1], is associated with higher hand performance 103 in free-ranging bonnet macaques, Macaca radiata. To this end, we determined the extent to which (a) the macaques exhibit laterality in hand usage in two 105 experimental unimanual and a bimanual food-reaching task, and (b) manual 106 laterality is associated with hand performance in an experimental hand-107 performance-differentiation task. We expected negative correlations between (a) 108 the performance of the preferred hand in the hand-performance-differentiation 109 task (measured as the latency in food extraction; lower latency = higher 110 performance), the preferred hand determined using the bimanual food-reaching 111 task, and the normalized difference in the performance between the two hands 112 (measured as the difference in the latency in food extraction between them 113 normalized by the latency in food extraction using the preferred hand), and (b) 114 the normalized difference in the performance between the two hands and the 115 manual specialization (measured as the absolute difference in the laterality in 116 hand usage between the unimanual and the bimanual food-reaching tasks; 117 lesser difference = higher manual specialization). 118

Subjects and Study Site 121
The subjects were 16 free-ranging bonnet macaques: 2 adult males -AM1 and 122 AM2, 1 subadult male -SM1, 4 juvenile males -JM1, JM2, JM3, and JM4, 8 123 adult females -AF1, AF2, AF3, AF4, AF5, AF6, AF7, and AF8, and 1 juvenile 124 female -JF1 (see Table 1), inhabiting the Chamundi Hill range in Mysore, India 125 (GPS coordinates: 2°14'41"N 76°40'55"E). We provided the macaques with 126 food-reaching tasks and observed the corresponding hand usage. We adhered to 127 the American Society of Primatologists (ASP) "Principles for the Ethical 128 Treatment of NonHuman Primates" and conducted the present study as a part of 129 an ongoing research project that was approved by the Institutional Animal Ethics 130 Committee (IAEC) at the University of Mysore (because we conducted our 131 research on individuals which (a) did not belong to an endangered or a protected 132 species, and (b) inhabited an unprotected land with an unrestricted public 133 access, our research work did not require permission from any other authority). 134 135 Experimental Procedure 136 We presented the macaques with 3 sets of 7 consecutive trials, that is, 21 trials, 137 of experimental unimanual and bimanual food-reaching tasks. Solving the 138 unimanual task required obtaining a grape from an unlidded wire mesh box 139 (dimensions: 7.5 cm X 7.5 cm X 17.5 cm; these dimensions allowed the usage 140 of only one particular hand at a time) fixed on a wooden platform (dimensions: 141 90 cm X 60 cm) with one hand ( Fig. 1A; Movie S1), whereas solving the 142 bimanual task required opening and supporting the lid of a lidded wire mesh box 143 with one hand and obtaining a grape with the other hand ( We then determined manual specialization using the formula: MS = abs. (HI 171 bimanual -HI unimanual). We determined the hand majorly used for taking the 172 food out of the box in the bimanual food-reaching task, which we referred to as 173 the 'preferred hand,' and the opposite hand, which we referred to as the 174 'nonpreferred hand' (previously,in Mangalam et al. [1], we referred to these as 175 the 'maneuvering' and the 'supporting' hand respectively). Moreover, we 176 determined the laterality in hand performance (LHP) in the hand-performance-177 differentiation task, using the formula: LHP = (latency in food extraction using 178 the nonpreferred hand -latency in food extraction using the preferred 179 hand)/latency in food extraction using the preferred hand. The obtained LHP 180 values ranged from -1 to + 1, indicating the normalized difference in the 181 performance between the two hands (w.r.t. the preferred hand). 182

Statistical Analysis 184
We used the Spearman's rank correlation test to determine the relationships 185 between (a) the latency in food extraction using the preferred hand and the 186 laterality in hand performance in the hand-performance-differentiation task, and 187 (b) the LHP in the hand-performance-differentiation task and the difference in 188 the HI values between the unimanual and the bimanual food-reaching tasks. 189 Moreover, we used a Mann-Whitney U-test to make sure that there was no 190 difference in the number of bouts between the two hands for taking all 7 grapes 191 out of the box, which could have influenced these relationships. 192

193
Results 194 Table 1 reports the raw data on hand usage for the macaques (whereas all 16 195 macaques responded to the unimanual and the bimanual food-reaching tasks, 196 only 10 macaques responded to the hand-performance-differentiation task 197 perhaps because of a lower motivation to solve a relatively more difficult and 198 time-consuming activity). We found strong negative correlations between (a) the 199 latency in food extraction using the preferred hand in the hand-performance-200 differentiation task and the laterality in hand performance (LHP) (rs= -0.772, n 201 = 10, p = 0.020; Fig. 2A), and (b) the LHP in the hand-performance-202 differentiation task and the manual specialization (rs= -0.752, n = 10, p = 203 0.033; Fig. 2B). There was no difference between the two hands in the number 204 of bouts for taking all 7 grapes out of the box in the hand-performance-205 differentiation task (U = 41.5, df = 9, p = 0.226). 206 207 Discussion 208 We examined whether the division of labor in hand usage, as described by 209 Mangalam et al. [1], is associated with higher hand performance in free-ranging 210 bonnet macaques. We found strong negative relationships between (a) the 211 performance of the preferred hand in the hand-performance-differentiation task 212 and the normalized difference in the performance between the two hands, and 213 (b) the normalized difference in the performance between the two hands in the 214 hand-performance-differentiation task and the manual specialization. These 215 correlations demonstrate that the macaques that exhibit a higher manual 216 specialization, show a greater difference in the performance associated with their 217 two hands, and also extract food faster as compared to those that exhibit 218 smaller differences. 219 220 On the one hand, the almost ubiquitous existence of manual asymmetries in 221 nonhuman primates is likely to have some ecological advantages, and even 222 more likely when there are underlying neurological asymmetries, as 223 demonstrated in capuchin monkeys [24][25][26][27] and chimpanzees [28][29][30]. On the 224 other hand, there may be some obvious disadvantages. Objects supposedly are 225 randomly located with respect to the sagittal plane of an individual (i.e., towards 226 the left or towards the right); this introduces difficulty in solving some tasks for 227 individuals having a bias for one particular side. Fagot and Vauclair [9] reviewed 228 studies on manual asymmetries in nonhuman primates and drew a distinction 229 between hand preference and manual specialization. According to them, hand 230 preference refers to the consistent usage of one hand to solve familiar, relatively 231 simple, and highly practiced tasks, and may not be necessarily accompanied by 232 an improvement in hand performance. In contrast, manual specialization refers 233 to the consistent usage of one hand to solve novel, relatively complex, and not-practiced tasks that require peculiar action patterns, and is necessarily 235 accompanied by an improvement in hand performance. Moreover, individuals 236 generally exhibit manual specialization only when the tasks involve cognitively 237 demanding manual actions. Thus, there exists a marked difference between 238 hand preference and manual specialization in terms of the resulting differences 239 in the performance of the two hands, which is evidently visible while considering 240 the forms and/or functions of manual asymmetries, as described by Mangalam 241 et al. [1]. The difference in the HI values between the unimanual and the 242 bimanual food-reaching tasks allowed us quantifying manual specialization as an 243 entity separate from hand preference (which an individual is likely to show 244 because of an inherent bias) and examining whether it is associated with a 245 higher difference in the performance between the two hands. 246

247
In a previous study [31], captive capuchin monkeys exhibited a weak, but 248 statistically nonsignificant, positive relationship between the strength of hand 249 preference and the corresponding hand performance in a unimanual and a 250 bimanual versions of the box task. The study acknowledged that the strength of 251 hand preference could have affected the timing of the movements, and so the 252 observed relationship. This was, however, not the case of the present study 253 because the hand-performance-differentiation task ergonomically forced the 254 macaques to use either the left or the right hand, which allowed measuring the 255 hand performance independent of any ceiling effects, i.e., it was unlikely to 256 prime any motor actions associated with the hand opposite to that of the 257 intended one. It provided a standard setup, which could be more widely used to 258 compare hand performance across individuals while minimizing the possibilities 259 of confounding effects. We suggest the development of such standard and 260 robust experimental setups which might help answering the prevailing questions 261 on manual asymmetries in nonhuman primates. 262 263 the nonpreferred (i.e., supporting) hand respectively; LHP indicates laterality in hand performance. 379