Intra- and intergroup vocal behavior in resident killer whales, Orcinus orca

Intra- and intergroup vocal behavior in resident killer whales, Orcinus orca Brigitte M. Weiß a Department of Behavioural Biology, University of Vienna, A-1090 Vienna, Austria Helena Symonds and Paul Spong OrcaLab, P.O. Box 258, Alert Bay, B.C., V0N 1A0, Canada Friedrich Ladich b Department of Behavioural Biology, University of Vienna, A-1090 Vienna, Austria Received 13 June 2007; revised 21 September 2007; accepted 25 September 2007 Vocal communication within and between groups of individuals has been described extensively in birds and terrestrial mammals, however, little is known about how cetaceans utilize their sounds in their natural environment. Resident killer whales, Orcinus orca, live in highly stable matrilines and exhibit group-specific vocal dialects. Single call types cannot exclusively be associated with particular behaviors and calls are thought to function in group identification and intragroup communication. In the present study call usage of three closely related matrilines of the Northern resident community was compared in various intra- and intergroup contexts. In two out of the three matrilines significant changes in vocal behavior depending both on the presence and identity of accompanying whales were found. Most evidently, family-specific call subtypes, as well as aberrant and variable calls, were emitted at higher rates, whereas low arousal call types were used less in the presence of matrilines from different pods, subclans, or clans. Ways in which the observed changes may function both in intra- and intergroup communication. 2007 Acoustical Society of America. DOI: 10.1121/1.2799907 PACS number s : 43.80.Ka WWA Pages: 3710 3716 I. INTRODUCTION Vocal communication within and between groups of individuals has been described extensively in birds and terrestrial mammals birds: e.g., Kroodsma and Miller, 1996; Radford, 2004; Beecher and Campbell, 2005; mammals: e.g., Seyfarth, 1987; Boughman and Wilkinson, 1998; McComb et al., 2000. However, little is known about how cetaceans utilize their sounds in their natural environment Janik, 2000, in particular, vocal interactions with conspecifics. Vocal signals relate to behavioral contexts in several species, mainly in humpback whales, Megaptera novaeangliae, bottlenose dolphins, Tursiops truncatus see review by Tyack, 2000; Janik, 2000, southern right whales, Eubalaena australis Clark, 1982, and beluga whales, Delphinapterus leucas Belikov and Belkovich, 2003. Recently, Saulitis et al. 2005 reported context-specific calls also in the AT1 subpopulation of mammal-eating killer whales or orcas Orcinus orca in southern Alaska. Unlike transient orcas, the fish-eating, resident orcas of the northeast Pacific live in exceptionally stable matrilineal units hereafter termed matrilines, where offspring of both sexes travel with their mothers lifelong Bigg et al., 1990; Ford et al., 2000. They are frequently vocal and possess a complex vocal system with group-specific dialects Ford, 1989, 1991; Yurk et al., 2002 that remain stable over decades Deecke et al., 2000 a Current address: Konrad Lorenz Forschungsstelle, Fischerau 11, A-4645 Grünau im Almtal, Austria. Electronic mail: a9400355@unet.univie.ac.at b Electronic mail: Friedrich.Ladich@univie.ac.at and reflect genetic relatedness Barrett-Lennard 2000. Closely related matrilines are referred to as pods Bigg et al., 1990 and share most or all of their call repertoire. Ford 1991 grouped all pods that share any call types or subtypes into acoustic clans; subclans further define clans through use of subclan-specific call types. Relative production rates of different call types and whistles vary with broad behavioral states of the entire group Ford, 1989, but in contrast to the AT1 transients, none of the residents call types correlate exclusively with any particular activity Ford, 1989. Rather than reflecting behavioral states, the discrete call repertoires are thought to function primarily to maintain cohesion and coordinate activities in intragroup contexts Ford, 1989, 1991. There is increasing evidence that the individually distinct signature whistles of bottlenose dolphins function as cohesion calls when individuals of a social group are separated Janik and Slater, 1998; Watwood et al., 2005. Signature whistles may even facilitate reunions between separated individuals, especially between calves and their mothers Smolker et al., 1993. Similarly, resident orca matrilines were recently found to increase the usage of family-specific call types immediately after the births of calves, suggesting that family-specific call types are of profound importance for maintaining cohesion within the matriline, in particular between mothers and their dependent offspring Weiß et al., 2006. Also, call type matching in vocal exchanges within matrilines suggests that the discrete call types of residents function in intragroup communication Miller et al., 2004b. 3710 J. Acoust. Soc. Am. 122 6, December 2007 0001-4966/2007/122 6 /3710/7/$23.00 2007 Acoustical Society of America

In social species vocal signals are commonly found to not only serve communication within, but also between groups, and call usage and structure frequently change with the social context e.g., Elowson and Snowdon, 1994; Smolker and Pepper, 1999; Hopp et al., 2001; Snowdon and de la Torre, 2002; Baker, 2004; Radford, 2005. Group size and composition are known to affect the use of stereotyped calls in several highly social species, e.g., African elephants Payne et al., 2003 and Northern right whales Parks and Tyack, 2005. Resident orcas are very social and matrilines regularly travel and interact together irrespective of relatedness or degree of call sharing, yet, intergroup communication has received little attention and has only come into focus recently. Riesch et al. 2006 described stereotyped whistle types that are shared throughout the Northern resident population and potentially serve in vocal communication even between members of different acoustic clans. Also, the call design of several discrete call types suggests that they are long-range communication signals with an active space exceeding by far the distances across which members of a matriline usually separate Miller, 2006 and the existence of multiple long-range call types suggests a role in intergroup communication. We thus suggest a significant role of discrete calls not only in intragroup, but also in intergroup, communication of resident orcas. To test this hypothesis, we analyzed call use of three Northern resident matrilines in intraand intergroup contexts, i.e., matrilines traveling alone or with other matrilines of different relatedness. In particular, we tested the following predictions: 1 Call use of focal matrilines changes with the presence or absence of other matrilines and 2 changes depend on the identity of the other matriline s. II. MATERIAL AND METHODS A. Study animals and data collection Johnstone Strait and adjacent waters off Vancouver Island, British Columbia, form the summer core area for the Northern resident community of orcas, which consists of more than 200 individually known orcas in three acoustic clans Bigg et al., 1990. The focus in this study was on three closely related matrilines, A12, A30, and A36, comprising the most commonly encountered pod, A1 Ford et al., 2000. In October 2002, they consisted of 7, 7, and 3 individuals, respectively Table I. Visual data were obtained at OrcaLab, located centrally in the study area 50 34 N and 126 42 W, and through a network of observers: OrcaLab volunteers stationed at field stations, other independent researchers, and whale watch operators. Data from all sources were integrated and summarized on a daily basis. The waterways were routinely surveyed with spotting scopes; visual observations were done on an opportunistic basis, whenever whales were seen or heard within the vicinity of a station. Upon sighting, the number and identity of individuals based on ID catalog Ford et al., 2000, group composition, group cohesion, direction of movement, and behavioral state travel, motionless, forage, or socialize were recorded. As long as whales TABLE I. Life history parameters of the individuals belonging to the three matrilines within the A1 pod in the studied timeframe. ID numbers and demographic data according to Ford et al. 2000. Matriline ID Sex Born Died Mother A12 A12 Female 1941 unknown A31 Male 1958 1997 A12 A33 Male 1971 A12 A34 Female 1975 A12 A55 Male 1989 A34 A62 Female 1993 A34 A67 Unknown 1996 A34 A74 Unknown 2000 A34 A30 A30 Female 1947 A2 A6 Male 1964 1999 A30 A38 Male 1970 A30 A39 Male 1975 A30 A50 Female 1984 A30 A54 Female 1989 A30 A72 Unknown 1999 A50 A75 Unknown 2001 A54 A36 A36 Female 1947 1997 A1 A32 Male 1964 A36 A37 Male 1977 A36 A46 Male 1982 A36 were within visual range, changes in any of the previous parameters, as well as times, when the whales passed key landmarks, were noted. Acoustic data were collected with a hydrophone network monitored at OrcaLab 24 h a day and year round. Whales were recorded on a two-channel audio cassette recorder Sony Professional Walkman WM-D6C or Sony TCD-D3 with up to six radio-transmitting, custom-made hydrophone stations overall system frequency response 10 Hz 15 khz whenever they were vocal see Weiß et al., 2006. Data collection was strictly land based and thus did not interfere with or disturb the whales. B. Acoustic analyses Focal matrilines were frequently observed and recorded with matrilines from different pods closely related matrilines, subclans, and clans. For investigating the intraand intergroup vocal behavior we selected recordings where focal matrilines were encountered in one of five clearly defined social contexts: 1 alone, 2 together with the other two A1 matrilines same pod, 3 in the company of matrilines belonging to a different pod within the same acoustic subclan same subclan, 4 in the company of matrilines belonging to a different subclan within the same clan other subclan, or 5 in the company of matrilines belonging to a different clan other clan. Alone referred to situations in which only the focal matriline was seen or heard within the same or adjacent hydrophone range s. A focal matriline was considered to be in the company of another matriline when both were observed within acoustic range of each other, were heading in the same direction and were engaged in the same behavior. Distances between matrilines traveling in company were estimated with the help J. Acoust. Soc. Am., Vol. 122, No. 6, December 2007 Weiß et al.: Orca vocal behavior and group composition 3711

TABLE II. Number of samples, calls and recording days of focal matrilines in varying social contexts. Matriline With n samples n calls n days A12... 10 983 7 A12 Other pod 6 570 3 A12 Other subclan 2 181 1 A12 Other clan 2 159 1 A30 15 1500 14 A30 Other pod 4 353 3 A30 Other subclan 2 186 1 A30 Other clan 6 550 4 A36 10 965 7 A36 Other pod 3 258 3 A36 Other subclan 4 366 2 A36 Other clan 9 810 6 A12+A30+A36 8 783 4 of landmarks and were typically well below 1000 m. We only used recordings for further analysis during which the spacing, direction of travel, and behavioral states of the involved matrilines were observed from shore or were reported from whale watching boats, and that allowed definite attribution of calls to the matrilines in a defined situation. This excluded night-time recordings as well as those where one or more additional matrilines were seen and/or heard within range of the same hydrophone as the defined matriline s. The selected recordings were obtained between 1989 and 2002 except for one recording of the A30 and B7 matrilines, that was obtained in August 2005. The predominant behaviors were traveling and/or foraging. Calls were classified according to Ford 1987, 1989, 1991 by simultaneous acoustic and visual inspection of sonagrams, generated with Cool Edit 2000 Syntrillium Software Corporation or Raven 1.2 Cornell Lab of Ornithology. Two call subtypes, N5iii and N9iv Weiß et al., 2006, were additionally distinguished because they were family specific to focal matrilines. C. Statistical analyses If more than 5% of calls were not both visually and acoustically recognizable because of poor signal-to-noise ratio, recordings were excluded from statistical analysis to avoid a bias towards call types of higher amplitude see Miller and Tyack, 2001. The remaining data were split into samples of 100 calls. Preferably, samples were chosen from different recording days. However, because selection criteria strongly reduced the number of usable samples in some of the defined social contexts, we also included recordings with less than 100, but a minimum of 75 calls. For the same reason, we sometimes used multiple samples from the same day, but as widely separated in time as possible and never more than three to maximize statistical independence of the data Table II. For each sample, we determined percentages of call use per call sub- type as well as the call rate n calls/minute/individual and the number of different call types used. Data were analyzed using the SPSS statistical program. As data clearly deviated from normal distribution Shapiro-Wilk, all parameters p 0.02, they were tested nonparametrically. Also, data were tested separately for each matriline, as basic call use differs somewhat between the three focal matrilines Miller and Bain, 2000; Weiß et al., 2006. Frequencies of call types and numbers were compared between single focal matrilines and focal matrilines in company using Mann-Whitney-U tests. Because calls could not be reliably attributed to the producing matriline when all three focal matrilines were recorded together, we did not compare recordings of the three matrilines together with those of the single matrilines, but rather with several averaged samples frequency of a given call type for A12 +A30+A36 divided by 3. In those cases, where call use did differ between the single and the company contexts, we conducted Kruskal-Wallis tests to further test for differences in call use depending on the identity of the company. Comparisons of call use between each single social context were not feasible due to an n below 5 in 6 of 9 of the company contexts. We did not consider alpha correction for multiple testing, because of an increased risk of type-ii error due to small sample sizes Nakagawa, 2004. Call types with rates of occurrence below 1% in any context were included in the category other for the given matriline. All statistical tests were two-tailed. FIG. 1. Call use of all three focal matrilines traveling on their own or with each other. ab, aberrant and var, variable. Bars show median percentage of total calls and first and third quartiles. Asterisks mark significance levels: *= p 0.05; = p 0.06; and n=8 alone and 9 together. 3712 J. Acoust. Soc. Am., Vol. 122, No. 6, December 2007 Weiß et al.: Orca vocal behavior and group composition

FIG. 2. Call use of the A12 matriline traveling on its own or with whales from different pods or sub- clans. ab., aberrant; var., variable; and imit., imitation. Bars show median percentage of total calls and first and third quartiles. Asterisks mark significance levels: *= p 0.05; ** = p 0.01; and n =10 alone and 10 with company. III. RESULTS Altogether, 81 samples totaling 7664 calls of focal matrilines on their own or in the company of other groups were of sufficient quality for statistical analysis Table II. Call patterns when matrilines were alone were comparable to those described by Miller and Bain 2000 and Weiß et al. 2006 for the three focal matrilines. With the exception of N3 calls and N10 calls, mean call use of the single A1 matrilines was very similar to that of the A1 matrilines traveling together Fig. 1. N3 calls made up a significantly smaller proportion of calls when all three A1 matrilines were together Mann-Whitney U test, n=17, U =9, p=0.008, while the use of N10 calls tended to increase in such situations Mann-Whitney U test, n=17, U=16, p =0.059. In the presence of more distantly or unrelated matrilines from other pods/clans, the A12 matriline was found to increase the use of the family-typical N5iii, as well as aberrant and imitation calls Fig. 2, Mann-Whitney U test, N5iii: n =20, U=22.5, p=0.035, aberrant: n=20, U=20, p=0.023, imitation: n=20, U=15, p=0.007. In each case, changes in call use were below 5%. Although we did not find any significant differences in call use of the A30 matriline traveling with or without company Fig. 3, they used the family typical N47 call 2 3 times more often in the presence of B-subclan for which two samples were available. The A36 matriline showed a number of distinct changes Fig. 4.Asin the A12 matriline, the family-typical call subtype, N9iv, was used significantly more often in the presence of other groups, which was also the case for variable calls Mann-Whitney U test, N9iv: n=26, U=25, p=0.003, variable: n=26, U =21.5, p=0.001. On the other hand, N1, N3, N7, N8 and N9i calls made up significantly higher portions of the call repertoire when the matriline was recorded on its own Mann-Whitney U test, N1: n=26, U=41.5, p=0.041, N3: n=26, U=24, p=0.002, N7: n=26, U=33, p=0.012, N8: n =26, U=32, p=0.01, N9i: n=26, U=34.5, p=0.014. With up to 10% change in call use, differences were more pronounced in the A36 matriline than in the A12 matriline. The use of some call types also differed depending on which group accompanied a focal matriline Fig. 5, Kruskal- Wallis test, A12 aberrant: n = 10, H = 5.595, p = 0.061, A36 N7: n = 10, H = 5.854, p = 0.054, A36 variable: n =10, H=6.014, p=0.049, which suggests that changes in call use may not only have been affected by the presence of other groups, but also by their identity. However, sample sizes in the different conditions were low and more detailed analyses were not feasible. Focal matrilines did not differ in their call rate n calls/ minute/individual nor in the number of different call types used in any of the contexts Kruskal-Wallis test, all p 0.1, Mann-Whitney U test, all p 0.1. FIG. 3. Call use of the A30 matriline traveling on its own or with whales from different pods or sub- clans. ab., aberrant and var., variable. Bars show median percentage of total calls and first and third quartiles. n=15 alone and 12 with company. J. Acoust. Soc. Am., Vol. 122, No. 6, December 2007 Weiß et al.: Orca vocal behavior and group composition 3713

FIG. 4. Call use of the A36 matriline traveling on its own or with whales from different pods or sub- clans. ab., aberrant and var., variable. Bars show median percentage of total calls and first and third quartiles. Asterisks mark significance levels: *= p 0.05. ** = p 0.01; and n=10 alone and 16 with company. IV. DISCUSSION FIG. 5. Use of a N7 calls and b variable calls by the A36 matriline in different social contexts focal matriline alone, with matrilines from the same subclan, another subclan or another clan. Bars show median percentage of calls and first and third quartiles. Numbers of samples appear above the bars. This study presents evidence that resident orca matrilines change their vocal behavior in intergroup contexts. Consistent with our predictions, percentages of call types used by focal matrilines depended on the presence or absence of additional matrilines in two out of three studied matrilines; findings for the third matriline were also consistent in key respects, though sample sizes were small and the changes were not statistically significant. The most consistent changes were increases in the use of family-specific call subtypes as well as variable and aberrant calls in the presence of orcas from other groups. Changes in call use were typically well below 10% and thus less pronounced than the changes observed in call use in another social context, i.e., after the birth of a calf Weiß et al., 2006. The focal matrilines differed considerably in the number of call types with emission rates affected by the social context. The A36 matriline showed significant changes in call use in half of their repertoire 7 of 14 call types, the A12 matriline to a considerably lesser extent 3 of 15 call types, and there were no statistically significant changes at all in the A30 matriline. However, their family typical N47 call was used 2 3 times as often in the presence of B-subclan matrilines and interestingly, changes in the A36s acoustic behavior were also strongest in the presence of matrilines from B-subclan. To some extent, the differences in call use may reflect low sample sizes for some matrilines in some contexts; however, it is also possible that they reflect different social roles arising from differences in associations and movement patterns. At least one of the three focal matrilines is present in the study area, almost daily, during each summer and fall Symonds and Spong, private communication. Changes in call use exhibited by the A1 matrilines thus may reflect differences in the manner in which each of the matrilines responds to intergroup situations involving the other, less commonly visiting Northern resident groups in the Johnstone Strait area, and they may underscore possible differing social roles within their own pod and community. Just how each of the A1 matrilines performs its role and specifically what these roles might be is beyond the scope of this study, however, the indication that matrilines within a pod have possible different roles should encourage further investigation. It also seems possible that some of the changes we observed reflect differences in the age and sex composition of individual matrilines. Indeed, the three focal matrilines do differ in this respect; the A36 matriline consisted of only one female and her three adult sons prior to the matriarch s death in 1997, and since then only of adult males, whereas the other two matrilines each added a new generation during the study period. Studies of other species show that vocal signals can convey not only individual or group-specific informa- 3714 J. Acoust. Soc. Am., Vol. 122, No. 6, December 2007 Weiß et al.: Orca vocal behavior and group composition

tion, but also age and sex-specific cues that may remain distinguishable even when transmitted over greater distances e.g. Green, 1981; Rendall et al., 2004; Blumstein and Munos, 2005. Animals may respond differently to calls of males and females e.g., Vicario et al., 2001; Miller et al., 2004a or may respond differently to signals depending on their own sex Rogers et al., 2006. It is plausible, therefore, that the differences in call use among our focal matrilines stemmed partly from different age or sex distributions in the focal or the accompanying matrilines. However, as virtually nothing is known about age or sex differences in the call use of wild orcas, this idea remains purely speculative. At least in some call types, changes in use seemed not only dependent on the mere presence of nonfocal matrilines, but to some degree on whether these nonfocal whales were from a pod within the same subclan, from a different subclan, or from an entirely different clan, i.e., whales that differ both in the degree of relatedness and of call type sharing. Although the focal matrilines share almost all call types with whales within the same subclan, they share few with those from a different subclan and none with whales from a different clan Ford, 1987, 1991. Studies in other species have shown that the degree of vocal sharing may play an important role in acoustic communication between groups and individuals. For instance, song sparrows, Melospiza melodia, were more likely to perceive a song as directed at them if the song was shared than if it was unshared Beecher and Campbell, 2005 ; and great tits, Parus major, responded differently to song types shared with neighbors and strangers Stoddard, 1996. Observations of primates are consistent with those for birds. Lemasson and Hausberger 2004 observed more vocal exchanges in Campbell s monkeys, Cercopithecus campbelli, that shared calls and suggested sharing to be important in advertising bonds. Complex vocal signals can serve multiple functions in inter-group behavior, such as cooperation, inter- and intrasexual assessment between groups e.g., Seddon, 2002, and call repertoire and complexity are often parameters used in mate choice see McGregor, 1992. The higher percentages of variable, aberrant and in part also imitation calls in intergroup contexts may reflect some of these vital aspects of social interactions. Variable and aberrant calls have been associated with situations of high arousal, e.g. during socializing Ford, 1989, 1991 and may reflect a more sexually charged situation, since whales from disparate groups are more likely to mate Barrett-Lennard, 2000. Ford 1989 also reported whales to be highly vocal when engaged in socializing i.e. showing physical contact, aerial displays etc.. However, the mere presence of other groups that were not engaged in active socializing, did not lead to an increase in the call rates of our focal matrilines. In contrast to states of high arousal, low arousal calls like N3 and N7 calls are heard most often during behaviours such as resting Ford, 1989; Symonds and Spong, private communication, so their tendency to occur more frequently in matrilines on their own might reflect a similar state of low arousal in this particular social context. Finally, the lack of changes in the majority of discrete call types may indicate that they serve the same functions in intra- and intergroup communication, such as directionality cueing and thus indicating one s location and direction of movement Miller, 2002. In conclusion, the presence and identity of accompanying matrilines significantly affected calling behavior of resident orca matrilines. The observed changes seem to reflect call functions in both intragroup, as well as intergroup, communication, and differences between matrilines hint at possible different social roles within the community. To get a better understanding of these roles, we will need extensive data sets of individual calling behavior along with precise behavioral observations. Both are currently extremely difficult to obtain, but provide potentially fruitful challenges for future research. ACKNOWLEDGMENTS The authors wish to thank Anna Spong and OrcaLab assistants for continuous recording and observation efforts. 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