Lateralization of spatial relationships between wild ...

Animal Behaviour xxx (2013) 1e7

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Lateralization of spatial relationships between wild mother and infant orcas, Orcinus orca Karina Karenina a, Andrey Giljov a, Tatiana Ivkovich a, Alexandr Burdin b, Yegor Malashichev a, c, * a b c

Department of Vertebrate Zoology, Faculty of Biology and Soil Sciences, Saint Petersburg State University, St Petersburg, Russia Kamchatka Branch of Pacific Institute of Geography, FED RAS, Petropavlovsk-Kamchatsky, Russia Department of Embryology, Faculty of Biology and Soil Sciences, Saint Petersburg State University, St Petersburg, Russia

a r t i c l e i n f o Article history: Received 28 June 2013 Initial acceptance 2 August 2013 Final acceptance 6 September 2013 Available online xxx MS. number: 13-00546R Keywords: boat approach calf position fear response killer whale lateralization motherinfant interaction Orcinus orca right hemisphere social laterality

Cooperative interactions have been argued to be a powerful factor mediating the evolution of lateralization in animals. Motherinfant asymmetric spatial relationships represent a case of social coordination among organisms. Although lateralized interactions between mothers and infants have been found in beluga whales, Delphinapterus leucas, whether this is the case in other cetaceans remains unknown. In the current study, we investigated mothereinfant spatial laterality, more specifically, the lateral biases in an infant’s position near its mother in wild orcas, Orcinus orca. Distances between the research boat and whales were categorized into three groups to test the influence of a potential threat on laterality expression. Observations on travelling individually identified mothereinfant pairs showed group-level preference for the infant to be on the mother’s right side when far from the boat. This bias reversed at close distance. At an intermediate distance, no significant side bias was found; however, when we considered only cases of apparent mothercalf pair avoidance of the boat for analysis, the left-sided bias was again observed. In contrast, when infants were socializing near mothers or when they followed older calves, the infants preferred the right side. We argue that these preferences are associated with righthemispheric advantage in social responses, while the shift from right-sided to left-sided bias in potentially threatening situations is caused by role reversal between mother and infant in determining their relative position in the dyad. Cetaceans seem to share with primates the pronounced lateralization of parentoffspring relationships. Ó 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

It has been suggested that when asymmetrical individuals need to coordinate their behaviour with each other, uniformity in side preferences within a population is advantageous (Ghirlanda & Vallortigara 2004; Vallortigara & Rogers 2005; Ghirlanda et al. 2009; MacNeilage et al. 2009). A particular case of social coordination in animals is parenteoffspring interactions, when two potentially lateralized individuals (e.g. a mother and an infant) need effective coordination with each other. Laterality in infant holding in human and nonhuman primates has been the subject of extensive research during the last few decades (reviewed in Harris 2010). Left-sided cradling preference has been found in humans of various cultures (Saling & Cooke 1984), as well as in great apes (Manning et al. 1994). A crucial role of hemispheric specializations

* Correspondence: Y. Malashichev, Department of Vertebrate Zoology, Faculty of Biology and Soil Sciences, Saint Petersburg State University, Universitetskaya nab., 7/9, St Petersburg 199034, Russia. E-mail addresses: [email protected], [email protected] (Y. Malashichev).

for lateral cradling bias has been suggested (e.g. Manning & Chamberlain 1990; Sieratzki & Woll 1996; Manning et al. 1997). For instance, infant holding on the left side of the body may be beneficial owing to the primary flow of visual information from a child to the mother’s right hemisphere (Manning & Chamberlain 1991), which is faster and more accurate at recognizing emotions and facial expressions (Ley & Bryden 1979; Strauss & Moscovitch 1981). Misinterpreting neutral faces as emotional is significantly less common in females when baby portraits are presented in the visual field consistent with the preferred cradling side (i.e. in the left visual hemifield in left holders; Huggenberger et al. 2009). Lefthanded cradling may bear an advantage for the infant who receives more maternal communication to the right hemisphere (Sieratzki & Woll 1996) and can see the more expressive left side of the mother’s face (Manning & Chamberlain 1991). It has been shown empirically that an infant has better visibility of its mother’s face when it is cradled in the mother’s left arm than when it is cradled in her right arm (Hendriks et al. 2011). The hypothesis of cerebral origin of cradling bias is consistent with the general evidence of the right-hemispheric superiority in human perception of social signals

0003-3472/$38.00 Ó 2013 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.anbehav.2013.09.025

Please cite this article in press as: Karenina, K., et al., Lateralization of spatial relationships between wild mother and infant orcas, Orcinus orca, Animal Behaviour (2013), http://dx.doi.org/10.1016/j.anbehav.2013.09.025

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K. Karenina et al. / Animal Behaviour xxx (2013) 1e7

(reviewed in Brancucci et al. 2009), but the trait is not unique to our species. The pivotal role of the left-eyeeright-hemisphere system in social behaviour has been found in vertebrates ranging from fish, amphibians and reptiles to birds and mammals (reviewed in: Vallortigara & Rogers 2005; Rogers et al. 2013). For instance, the right-hemisphere advantage has been clearly shown in sheep, Ovis aries, when recognizing conspecific faces (Peirce et al. 2000). Despite considerable evidence of social lateralization in different vertebrate taxa, studies on lateralized parenteoffspring interactions have been confined mostly to primates. Only in ungulates has one specific aspect of motherinfant interactions, suckling, been studied in terms of lateralization. A foal’s preference for suckling side was determined in loose-housed domestic horses, Equus caballus (Komárková & Bartosová 2013), and captive zebras, Zebra spp. (Pluhá cek et al. 2013). Both studies found no populationlevel preference in suckling side, with only about one-third of foals showing individual biases. However, suckling may not be a representative behaviour for motherinfant laterality: when suckling, the foal is focused on the process of feeding (Komárková & Bartosová 2013), and the foal’s position is unlikely to be determined by the perception of the mother. Perhaps, other aspects of the motherinfant interactions in ungulates would be more suitable for laterality estimation. Thus, the lack of studies on nonprimate mammals does not allow researchers to trace the evolutionary origins of parentinfant lateralization. Much like primates, cetaceans are highly social, large-brained and slow-developing animals with close and long-lasting bonds between mother and offspring. Thus, cetaceans can serve as an excellent model to provide new insights into understanding the nature of lateralization in spatial relationships between mother and infant. Already, cetaceans have been shown to be lateralized in many aspects of their behaviour, such as foraging (Silber & Fertl 1995; Woodward & Winn 2006; Canning et al. 2011), rotational swimming (Sobel et al. 1994; Marino & Stowe 1997), social interactions (Sakai et al. 2006; Karenina et al. 2013b), visual discrimination and object examination (Kilian et al. 2005; Delfour & Marten 2006; Karenina et al. 2010b; Blois-Heulin et al. 2012; Siniscalchi et al. 2012). Several anatomical features, such as laterally placed eyes, complete decussation of the optic fibres and relatively strong isolation of brain hemispheres (less developed corpus callosum; Supin et al. 1978; Ridgway 1986; Tarpley & Ridgway 1994; Marino et al. 2004), make cetaceans a perfect group for studying laterality in visually guided behaviours and underlying cerebral lateralization (Kilian et al. 2005; Karenina et al. 2010b; Blois-Heulin et al. 2012; Siniscalchi et al. 2012). Recent studies (Karenina et al. 2010a, 2013b) have established that beluga whales, Delphinapterus leucas, show individual and population lateralization in mothereinfant spatial relations. Beluga infants prefer to swim and rest on the mother’s right side (Karenina et al. 2010a, 2013b). When leaving their mothers, beluga calves prefer to swim to the right of groups of older juveniles. Social variables, such as presence and position of nearby individuals, had no influence on laterality. The lateral bias in mothereinfant pairs was assumed to be caused by calves’ right brain hemisphere specialization for social processing (Karenina et al. 2013b). To date, beluga whales are the only cetacean species studied from the standpoint of mothereinfant spatial laterality. In the present study we explored mothereinfant spatial laterality in wild orcas, Orcinus orca. It remains largely unclear how environmental factors influence the expression of mothereinfant laterality. Here we focus on the effect of a potential threat on the asymmetric infant’s position in orca mothereinfant pairs. Human disturbance has been repeatedly shown to affect cetacean behaviour (e.g. Corkeron 1995; Nowacek et al. 2001; Constantine et al. 2004; Stensland & Berggren 2007). Vessel

traffic, and especially targeted vessel approach (e.g. during whale watching), seems to represent the most common source of human disturbance for cetaceans. Human activities may induce various avoidance tactics, such as adopting a less predictable path or swimming faster (horizontal avoidance), and altering or lengthening the duration of dives (vertical avoidance; Williams et al. 2002). Orca is one of the few species on which the impact of vessel traffic has been quantified (Williams et al. 2002, 2006; Lusseau et al. 2009): orcas respond to an approaching boat by adopting less predictable erratic swimming paths consistent with horizontal avoidance similar to that used against predators (Williams et al. 2002). Thus, the approach of a boat could be likened to a threatening situation for orcas and therefore serve as a model, in which the impact of environmental cues on whale laterality expression can be tested. In the present study, we assessed the influence of an approaching boat on laterality in orca mothereinfant pairs. Taking into account that parental stress leads to significant shifts in infantcradling bias in humans (Weatherill et al. 2004; Reissland et al. 2009; Suter et al. 2011), we hypothesized that, in orcas, laterality in mothereinfant pairs would be significantly affected by boat approach. To test this hypothesis, we analysed left/right biases in calves’ position when travelling side by side with their mothers at different distances to a research boat. METHODS Data Collection The data were collected as part of a long-term orca project (Far East Russia Orca Project, FEROP) conducted in Avacha Gulf of Kamchatka, Northwest Pacific since 1999. The observational procedures applied in the study are described elsewhere (Ivkovich et al. 2010; Filatova et al. 2012). The behavioural observations were made on resident orcas (fish-eating ecotype) in JulyeAugust 2011. We used small inflatable boats to approach groups of whales at a distance of about 100 m for observations, photography and video recordings. Whales were approached at a slow speed, moving in parallel with a group’s travel direction, and the group was allowed to pass after the necessary data were collected. We used digital video cameras to record surface behaviour of females with infants when they were less than one whale length from the other (Fig. 1a, b). We recorded rare occurrences of an infant leaving its mother and accompanying an older infant in a separate data set. We included in the analysis only those situations when two infants formed a pair in the absence of their mothers nearby (e.g. while mothers were foraging). For pairs consisting of two infants only, we also used data obtained in previous field seasons (2005e2010) to increase the sample size of such rare events. Using a high-resolution camera with a long focus lens, we took pictures of each individual for identification. Photoidentification was based on a set of natural markings (e.g. colour pattern of saddle patch and eye patch, fin shape and scars on the body and fins; Würsig & Jefferson 1990). Comparison of photos with the FEROP database allowed us to check relatedness between individuals in a pair and to determine each infant’s age (Ivkovich et al. 2010). The following mothereinfant behaviours were studied: travelling, socializing and boat avoidance (based on Barrett-Lennard et al. 1996; Erbe 2002; Filatova et al. 2009). Whales were considered to be travelling when they moved, making more than five breaths in the same direction at the same speed. Socializing included various social interactions featured by aerial displays (e.g. breaching, flipper and fluke slapping, rolling over each other and sexual interactions; Fig. 1c). Socializing was usually accompanied by little or



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Figure 1. Lateral position of an orca infant relative to its mother: (a) newborn AV058d travelling on the right side of the mother AV058; (b) juvenile AV096a travelling on the left side of the mother AV096; (c) calf AV397a socializing on the right side of the mother AV397; (d) motherinfant pair, AV214 and AV214a, accompanied by male AV280 on the right side. Photoidentification method is described elsewhere (Würsig & Jefferson 1990; Ivkovich et al. 2010).

no consistent displacement in space. If avoidance behaviour (sudden and persistent change in travel direction, usually away from the boat) was recorded, we ceased our approach. We used a marine binocular with built-in reticle scales to estimate the approximate distance between focal whales and the research boat, which we then classified into one of three distance categories: far (160e180 m), which was considered to have minimal effect on whale behaviour; close, when the orcas came extremely close ( 0.111) with only one pair demonstrating a right-sided preference (z ¼ 3.32, P < 0.001). Mean duration of left-sided and rightsided bouts differed only for one mothereinfant pair (Manne Whitney U test: U ¼ 12e259.5, N1 ¼ N2 ¼ 6e25, P > 0.321), which showed longer left-sided bouts (U ¼ 33, N1 ¼ N2 ¼ 14, P ¼ 0.003). We estimated individual laterality at close distances for four motherinfant pairs, and all of them showed a significant leftsided bias in calves’ position (z ¼ 2.21e3.06, P < 0.021). There was no significant influence of infant age on laterality at far distances (Spearman rank correlation: rS ¼ 0.45, N ¼ 7, P ¼ 0.310) or intermediate distances (rS ¼ 0.19, N ¼ 11, P ¼ 0.570). Relative positioning of the mother and infant recorded during the pair’s avoidance of the research boat showed significant prevalence of infants situated to the left (10 of 11; binomial test: z ¼ 2.41, P ¼ 0.012). In contrast, when an infant was socializing near its mother, it was situated on its mother’s right side in the majority of pairs (11 of 13; binomial test: z ¼ 2.22, P ¼ 0.022). Pairs that were formed by two infants travelling without their mothers showed that the younger infant tended to escort the older infant on the right side (14 of 16; binomial test: z ¼ 2.75, P ¼ 0.004).

DISCUSSION The present study demonstrates that spatial laterality exists in wild orca mothereinfant pairs. At far distances (160e180 m between whales and the research boat), we found a group-level preference for right-sided infant position. This preference was stable over time with most pairs showing the right-sided preference at the individual level. These results for far distances from the boat should most closely represent laterality in common nonthreatening situations. Notably, beluga whales also have the same directional bias in mothereinfant laterality (Karenina et al. 2010a, 2013b). The data on belugas were obtained using observations from the shore and aerial photography, both with minimized disturbance to the subjects, similar to our far distance data points. Congruent findings in beluga (Monodontidae) and orcas (Delphinidae) suggest that the right-sided position might be preferable for cetacean infants in nonthreatening situations generally, but studies in other taxa should be conducted before conclusions are drawn. Lateral bias of an infant relative to its mother was significantly affected by the distance to the research boat. At intermediate distances, there was no significant group preference, whereas at close distances, we observed a predominance of infants situated on the mother’s left side. Intermediate and close distances were considered to be increasingly stressful for motherinfant pairs, consistent with previous results showing an increase in orca’s avoidance response at approach distances of less than 100 m (Williams et al. 2002). Hence, we expect that the changes in spatial laterality caused by boat approaches should reflect the behavioural response to a potential threat, which increases as the distance to the boat decreases. The predator avoidance analogy has been used to interpret the behaviour of orcas that are approached by a vessel (Williams et al. 2002). We thus hypothesize that the shift in an infant’s position from right side to left side of its mother, found in

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the case of boat approach, will also be observed when a motherinfant pair evades an approaching predator. The wide intermediate distance category used in the present study, most likely included data from motherinfant pairs in which both members of the pair were affected and not affected by the presence of the research boat; these differences could depend on a variety of factors, such as individual experience with a boat, group composition, and so forth. Therefore, only the extreme distances (far and close) clearly illustrate the influence of the boat approach. In the majority of pairs, the right-sided infant position was observed far away from the boat and the left-sided position was observed at close distances. The nonbiased infant position at intermediate distances more likely reflects the heterogeneity of data owing to the wide category margins rather than the real absence of laterality. The right-sided preference appeared at intermediate distances when an infant was socializing near its mother, which can be considered an unstressed behaviour. In contrast, the left-sided bias in infant position occurred at intermediate distances when avoidance of the research boat was recorded. This provides further support for the hypothesis that the shift to the left-sided infant position is caused by threatening/dangerous situations, such as a boat’s close proximity. That the same pairs displayed different patterns of spatial laterality in different contexts may indicate that this laterality has a functional significance. The intrapair origin of the spatial laterality in the present study is additionally confirmed by the result that neither the presence nor the position (left/right) of other whales accompanying the pair influenced the side preference. So why is the right-sided infant position preferable in nonthreatening situations, whereas the left-sided position is preferred in cases of threat? The response to a predator has been found to be lateralized in many vertebrates (Lippolis et al. 2002, 2005, reviewed in Rogers et al. 2013). We found no difference in the infant’s positional bias when the pairs were approached from either their left or right side. Thus, mothereinfant laterality was not skewed by their lateralized perception of the boat, but it was influenced by the presence of the boat itself. One distinctive feature of cetacean calves is their early spatial independence from mothers (Mann & Smuts 1998, 1999; Gibson & Mann 2008; Hill 2009; Stanton et al. 2011). In beluga whale motherinfant pairs, the infant plays a dominant role in position choice (Hill 2009) and is responsible for laterality (Karenina et al. 2010a, 2013b). We suggest that orca calves do the same in nonthreatening situations; that is, they prefer to be on their mothers’ right side. The change of laterality in potentially threatening situations, on the other hand, may be caused by a mother’s dominant role in positioning relative to the infant. The right-sided preference was maintained when the infant followed an older infant, which might indicate that, unlike mothers, such temporary companions do not affect the spatial laterality in the pair. The mother and the infant may both prefer to keep the other on the left side, but swimming together makes this possible only for one of the pair. Probably, who maintains the preferable position in the pair depends on the situation: when following its mother in nonthreatening circumstances the infant has control of the position, while in potentially threatening situations the mother takes the lead. Keeping the other individual on the left side may be preferable for both mothers and infants, because such a position improves the flow of sensory information from the partner to their right brain hemisphere. The right-hemispheric advantage in social interactions, often manifested in the preferential use of the contralateral (left) eye, has been shown in a wide variety of vertebrates, including cetaceans (reviewed in: Brancucci et al. 2009; Rosa Salva et al. 2012). For instance, wild Indo-Pacific bottlenose dolphins, Tursiops aduncus, tend to use the left eye to see their partners during social contact such as flipper rubbing (Sakai et al.


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2006). Preferential left-eye use has been strongly argued to cause the right-side preference found in beluga calves following their mothers or older calves (Karenina et al. 2010a, 2013b). The uniformity of social lateralization pattern among vertebrate taxa allows us to suggest that the side biases in orca motherinfant interactions are due to right-hemisphere advantage in the recognition of social cues (e.g. Vallortigara 1992; Peirce et al. 2000; Brancucci et al. 2009; MacNeilage et al. 2009; Karenina et al. 2013a). Visual object examination and discrimination have been found to be lateralized in different cetacean species (Kilian et al. 2005; Delfour & Marten 2006; Karenina et al. 2010b; Blois-Heulin et al. 2012; Siniscalchi et al. 2012). However, we cannot rule out a possible role of acoustic and tactile communication in the origination of the observed laterality. Pinnipeds, for instance, have a left-eareright-hemisphere advantage, which they use for processing conspecific vocalizations (Böye et al. 2005). Population-level biases in infant cradling and holding have been found in human and nonhuman primates (reviewed in Manning et al. 1994; Hopkins 2004; Harris 2010). Primates and cetaceans share slow development and strong long-term bonds between mother and offspring. The pronounced motherinfant spatial laterality in both primates and distantly phylogenetically related cetaceans show that, at least in mammals with long periods of infant dependency, lateralized motherinfant relationships may provide some benefits. Altogether, the results on cetaceans (Karenina et al. 2010a, 2013b, this study) indicate that stable laterality in motherinfant interactions is not a unique primate characteristic and suggest potential phylogenetic continuity of this phenomenon across mammalian species. Acknowledgments We are grateful to Mikhail Nagaylik, Mikhail Guzeev, Ekaterina Borisova and Anton Biatov for their valuable help in the field work. This research was supported by the Federal Grant-in-Aid Program ‘Human Capital for Science and Education in Innovative Russia’ (Governmental Contract No. P2379), the Whale and Dolphin Conservation (WDC) and the Rufford Maurice Laing Foundation. We also thank Erich Hoyt for organizational help and Andrea L. Liebl for thoughtful comments on the manuscript and English style corrections. Supplementary Material Supplementary material for this article is available, in the online version, at http://dx.doi.org/10.1016/j.anbehav.2013.09.025. References Austin, N. P. & Rogers, L. J. 2012. Limb preferences and lateralization of aggression, reactivity and vigilance in feral horses, Equus caballus. Animal Behaviour, 83, 239e247. Barrett-Lennard, L. G., Ford, J. K. & Heise, K. A. 1996. The mixed blessing of echolocation: differences in sonar use by fish-eating and mammal-eating killer whales. Animal Behaviour, 51, 553e566. Blois-Heulin, C., Crével, M., Böye, M. & Lemasson, A. 2012. Visual laterality in dolphins: importance of the familiarity of stimuli. BMC Neuroscience, 13, 9. Böye, M., Güntürkün, O. & Vauclair, J. 2005. Right ear advantage for conspecific calls in adults and subadults, but not infants, California sea lions (Zalophus californianus): hemispheric specialization for communication? European Journal of Neuroscience, 21, 1727e1732. Brancucci, A., Lucci, G., Mazzatenta, A. & Tommasi, L. 2009. Asymmetries of the human social brain in the visual, auditory and chemical modalities. Philosophical Transactions of the Royal Society B, 364, 895e914. Canning, C., Crain, D., Eaton, T. S., Nuessly, K., Friedlaender, A., Hurst, T., Parks, S., Ware, C., Wiley, D. & Weinrich, M. 2011. Population-level lateralized feeding behaviour in North Atlantic humpback whales, Megaptera novaeangliae. Animal Behaviour, 82, 901e909.

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