Alexandr M. Burdin

Call diversity in the North Pacific killer whale populations: implications for dialect evolution and population history

Although killer whale, Orcinus orca, dialects have been studied in detail in several populations, little attempt has been made to compare dialect characteristics between populations. In this study we investigated geographical variation in monophonic and biphonic calls among four resident populations from the North Pacific Ocean: Northern and Southern residents from British Columbia and Washington State, southern Alaska residents, and eastern Kamchatka residents. We tested predictions generated by the hypothesis that call variation across populations is the result of an accumulation of random errors and innovation by vertical cultural transmission. Call frequency contours were extracted and compared using a dynamic time-warping algorithm. We found that the diversity of monophonic calls was substantially higher than that of biphonic calls for all populations. Repertoire diversity appeared to be related to population size: in larger populations, monophonic calls were more diverse and biphonic calls less diverse. We suggest that the evolution of both monophonic and biphonic calls is caused by an interaction between stochastic processes and directional selection, but the relative effect of directional selection is greater for biphonic calls. Our analysis revealed no direct correlation between call repertoire similarity and geographical distance. Call diversity within predefined call categories, types and subtypes, showed a high degree of correspondence between populations. Our results indicate that dialect evolution is a complex process influenced by an interaction among directional selection, horizontal transmission and founder effects. We suggest several scenarios for how this might have arisen and the implications of these scenarios for call evolution and population history.

THE STRUCTURE OF THE DISCRETE CALL REPERTOIRE OF KILLER WHALES ORCINUS ORCA FROM SOUTHEAST KAMCHATKA

ABSTRACT The problem of categorization arises in any classification system because classes should be discrete while the characteristics of most natural objects and aspects of nature are more or less gradual. In systematics, this problem usually is solved by creating several levels of categories, such as class, order, family, genus and species. In the existing killer whale discrete call classification, only two levels occur—call type and call subtype. In this paper we describe structural categories at a broader level than call type in the discrete sounds of killer whales and compare these categories between and within vocal clans in a community of resident killer whales from Southeast Kamchatka, Russian Far East, and also with killer whales outside this community. We found four main classes of discrete calls in the repertoire of resident killer whales from Southeast Kamchatka. The calls of Southeast Kamchatka transient killer whales and Sakhalin killer whales do not fall into these classes. This suggests that the resident killer whale community from Southeast Kamchatka has some rules defining the structure of calls which are typical for this community. Consequently, all resident killer whales from Southeast Kamchatka can be said to share the same vocal tradition.

Lateralization of spatial relationships between wild mother and infant orcas, Orcinus orca

Cooperative interactions have been argued to be a powerful factor mediating the evolution of lateralization in animals. Mother−infant 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 mother–infant spatial laterality, more specifically, the lateral biases in an infants 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 mother–infant pairs showed group-level preference for the infant to be on the mothers 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 mother−calf 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 right-hemispheric 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 parent−offspring relationships.

Usage of monophonic and biphonic calls by free-ranging resident killer whales (Orcinus orca) in Kamchatka, Russian Far East

Killer whale discrete calls include types containing an overlapping high-frequency component (biphonic calls) and types without an overlapping high-frequency component (monophonic calls). In the resident killer whales of the Northeast Pacific, biphonic discrete calls exhibit higher source levels than monophonic calls, which suggests different active space and consequently different functions for monophonic and biphonic call types. In this study we investigate the potential communicative functions of monophonic and biphonic discrete calls produced by killer whales from Kamchatka (Northwest Pacific). We analyze how the usage of these calls depends on the number of pods present in the area and type of activity. Our results show that the usage of monophonic and biphonic calls in Kamchatkan killer whales depends on the number of pods in the area and is less dependent on the type of activity. Biphonic calls are more common when more than one pod is present in the area and could therefore function as markers of pod and matriline affiliation, serving mainly as cohesion signals. Monophonic calls dominated the vocalizations when a single pod was present, while in the presence of more than one pod both categories were used in equal proportions.

Is killer whale dialect evolution random

The killer whale is among the few species in which cultural change accumulates over many generations, leading to cumulative cultural evolution. Killer whales have group-specific vocal repertoires which are thought to be learned rather than being genetically coded. It is supposed that divergence between vocal repertoires of sister groups increases gradually over time due to random learning mistakes and innovations. In this case, the similarity of calls across groups must be correlated with pod relatedness and, consequently, with each other. In this study we tested this prediction by comparing the patterns of call similarity between matrilines of resident killer whales from Eastern Kamchatka. We calculated the similarity of seven components from three call types across 14 matrilines. In contrast to the theoretical predictions, matrilines formed different clusters on the dendrograms made by different calls and even by different components of the same call. We suggest three possible explanations for this phenomenon. First, the lack of agreement between similarity patterns of different components may be the result of constraints in the call structure. Second, it is possible that call components change in time with different speed and/or in different directions. Third, horizontal cultural transmission of call features may occur between matrilines.

Dependence of killer whale (Orcinus orca) acoustic signals on the type of activity and social context

We investigated the influence of the type of activity and the social context on the proportion of four different structural categories of stereotyped calls in the acoustic communication of Kamchatkan killer whales. Using generalized linear models, we described the dependence of each sound category on the type of activity, the number of killer whale pods and the presence of mixed-pod groups. We found that the proportion of different sound categories depended on the number of pods and the presence of mixed-pod groups, while the type of activity did not affect the proportion of sounds of different categories. Based on the observed differences we suggest that biphonic and high-frequency monophonic calls are mainly used as family and pod markers, and help to track the position of family members at long ranges, and low-frequency monophonic calls are used as close-range intra-group signals to maintain contact between pod members in the conditions of limited underwater visibility.

Horizontal transmission of vocal traditions in killer whale (Orcinus orca) dialects

Unlike most other mammals, killer whales are capable of vocal learning and learn the dialect of their natal pod from their mothers. The classical model of killer whale dialect development suggests that the repertoire of calls is learned only “vertically” from mother to offspring, and calls evolve gradually with time by random drift caused by the accumulation of copying errors. However, some observations suggest that not only “vertical” (from mother to offspring) vocal learning can occur in killer whales, but also “horizontal” (between adult animals). In this study we analyzed the distribution of different call types and similarity of calls from the same type in different pods of killer whales from Kamchatka waters to estimate the probability of existence of interpod horizontal transmission of vocal traditions in killer whales. We found that the degree of similarity of K1 calls and K5 calls in different pods can differ. This situation contradicts the classical hypothesis and is possible in two cases: if different call types change with various speed in different pods, or if horizontal transmission of call features takes place. The distribution of K4 and K10 call types across pods also suggests the existence of horizontal transmission: K4 calls occur in the dialects of five of ten pods, and K10 calls, in six of ten pods, but only one pod has both K4 and K10 calls. Our results suggest that the real picture of the distribution of call features and call types in killer whale dialects contradicts the classical hypothesis of killer whale dialect evolution through the accumulation of copying errors.

The function of multi-pod aggregations of fish-eating killer whales (Orcinus orca) in Kamchatka, Far East Russia

In fish-eating North Pacific killer whales, large multi-pod aggregations of up to 100 animals often occur. These aggregations are thought to be reproductive gatherings where mating between members of different pods takes place. However, killer whales are social animals, and the role of these aggregations might also be establishing and maintaining social bonds between pods. Alternatively, it is also possible that multi-pod aggregations are in some way connected with foraging or searching for fish. In this study of killer whales in the western North Pacific, we describe multi-pod aggregations quantitatively and suggest their functional role in the life of fish-eating killer whales. We show that foraging is rare in multi-pod aggregations, whether inter-clan or intra-clan, and thus they are unlikely to play an important role in cooperative foraging. Socialising occurs more frequently in inter-clan rather than in intra-clan aggregations, which suggests the higher arousal level and possible mating during inter-clan aggregations. In summary, multi-pod aggregations of Kamchatka killer whales might be both reproductive assemblages and “clubs” of some kind in which whales gather to establish and maintain social bonds.

Reproductively isolated ecotypes of killer whales Orcinus orca in the seas of the Russian Far East

Two ecotypes of killer whales—fish-eating and mammal-eating—have been found in the seas of the Russian Far East, but confirmation of their status required genetic studies of animals with known phenotype and foraging specialization. In this paper we combine the results of the analysis of nuclear genetic markers, isotopic composition of tissues and phenetic feature (shape of the saddle patch) of killer whales from different regions of Far Eastern seas. Analysis of allelic composition of 9 microsatellite loci of the nuclear DNA divided the samples into two distinct clusters with the divergence between them high enough to indicate reproductive isolation. The content of nitrogen stable isotope 15N in tissues of whales from the first cluster was significantly lower than that of the second cluster. The difference of δ15N values between individuals from different clusters was about 3‰, which corresponds to the difference between adjacent trophic levels. Apparently, the first cluster comprised fish-eating, and the second—mammal-eating animals. The ratio of saddle patch shape types also differed between the clusters. Whales from the first cluster had five types of patch shape in different proportions, while whales from the second cluster had only “smooth” saddle patches. The differences between the clusters were statistically significant. Thus, killer whales from the seas of the Russian Far East comprise at least two reproductively isolated clusters with stable ecological and morphological differences, that is, two different ecotypes—fish-eating and mammal-eating. Different ecotypes of killer whales should be managed separately during abundance surveys, monitoring, evaluation of human impact and estimates of total allowed takes from the wild populations.

Social complexity and cultural transmission of dialects in killer whales

Many social animals have cultural traditions that may shape their societies while the social structure can in turn influence how the culture is acquired. Killer whales possess culturally transmitted dialects. The divergence of dialects was thought to occur simultaneously and consistently with the gradual fission of matrilines. In this paper we compare the social associations across matrilineal units, Bayesian phylogeny of dialects and similarity of particular syllables to test whether dialects affect social structure and whether associations or common origin define similarity of call types. We found that neither phylogeny of dialects nor similarity of syllables was correlated to associations between matrilineal units, but similarity of syllables was correlated to phylogeny of dialects for four of the six syllables analysed. The complexity and fluidity of social ties between matrilineal units and the variation in cultural transmission patterns produce a complex relationship between the social network and the socially learned vocalizations.