Killer whale innovation: teaching animals to use their creativity upon request.

Thinking flexibly is a skill that enables animals to adapt to changing environments, which enhances survival. Killer whales, Orcinus orca, as the ocean apex predator display a number of complex cognitive abilities, especially flexible thinking or creativity when it comes to foraging. In human care, smaller dolphins and other marine mammals have been trained to think creatively while under stimulus control. The results of these previous studies have demonstrated that bottlenose dolphins, Tursiops truncatus, can create original behaviors in response to an innovative cue. We trained and tested a total of nine killer whales from two different facilities on the innovate concept, using the same methodology. The killer whales ranged in age from 5 to 29 yrs with 4 females and 5 males. The results indicate that the killer whales demonstrated high fluency, originality, some elaboration, and flexibility in their behaviors. Individual variability was observed with younger animals demonstrating more variable behaviors as compared to the older animals. Males seemed to display less complex and lower energy behaviors as compared to females, but this impression may be driven by the age or size of the animal. These results support existing evidence that killer whales are dynamic in their thinking and behavior.

Social interaction analysis in captive orcas (Orcinus orca).

The management of socially complex species in captivity is challenging. Research on their social behavior improves our understanding of interactions in captive animals and captive-group management. We conducted a detailed analysis of social relationships shown by the orcas kept at Loro Parque zoo and their tendency to reconcile after aggressive episodes. Affiliative interactions were the most frequent social activities compared to agonistic or sexual interactions. Within affiliative behaviors, we documented the pattern "gentle tongue bite", where an animal touches the other's tongue with his teeth but does not bite it. Affiliative interactions between a specific pair of orcas occurred significantly more often than expected by chance, and together with low levels of agonistic interactions, indicated particular affinity between some individuals. The most frequently observed low-level agonistic relationship was that of the two older males (Tekoa-Keto); however, they also showed frequent sexual and affiliative interactions. Sexual-like behaviors (pursuit, mount, and penis between males) were found in both sexes. Finally, the observed corrected conciliatory tendency (31.57%) was within the range described for other primate and cetacean species. This study provides a systematic way to assess social interactions as well as conflict management strategies in cetaceans housed in zoos and zoo-like facilities and may help to improve animal welfare and management of animals in controlled environments.

Evidence for discrimination between feeding sounds of familiar fish and unfamiliar mammal-eating killer whale ecotypes by long-finned pilot whales.

Killer whales (KW) may be predators or competitors of other cetaceans. Since their foraging behavior and acoustics differ among populations ('ecotypes'), we hypothesized that other cetaceans can eavesdrop on KW sounds and adjust their behavior according to the KW ecotype. We performed playback experiments on long-finned pilot whales (Globicephala melas) in Norway using familiar fish-eating KW sounds (fKW) simulating a sympatric population that might compete for foraging areas, unfamiliar mammal-eating KW sounds (mKW) simulating a potential predator threat, and two control sounds. We assessed behavioral responses using animal-borne multi-sensor tags and surface visual observations. Pilot whales barely changed behavior to a broadband noise (CTRL-), whereas they were attracted and exhibited spyhops to fKW, mKW, and to a repeated-tonal upsweep signal (CTRL+). Whales never stopped nor started feeding in response to fKW, whereas they reduced or stopped foraging to mKW and CTRL+. Moreover, pilot whales joined other subgroups in response to fKW and CTRL+, whereas they tightened individual spacing within group and reduced time at surface in response to mKW. Typical active intimidation behavior displayed to fKW might be an antipredator strategy to a known low-risk ecotype or alternatively a way of securing the habitat exploited by a heterospecific sympatric population. Cessation of feeding and more cohesive approach to mKW playbacks might reflect an antipredator behavior towards an unknown KW ecotype of potentially higher risk. We conclude that pilot whales are able to acoustically discriminate between familiar and unfamiliar KW ecotypes, enabling them to adjust their behavior according to the perceived disturbance type.

Consequences of culturally-driven ecological specialization: Killer whales and beyond.

Culturally-transmitted ecological specialization occurs in killer whales, as well as other species. We hypothesize that some of the remarkable demographic and ecological attributes of killer whales result from this process. We formalize and model (using agent-based stochastic models parametrized using killer whale life history) the cultural evolution of specialization by social groups, in which a narrowing of niche breadth is spread and maintained in a group through social learning. We compare the demographic and ecological results of cultural specialization to those of a similar model of specialization through natural selection. We found that specialization, through either the cultural or natural selection routes, is adaptive in the short term with specialization often increasing fitness. Generalization, in contrast, is rarely adaptive. The cultural evolution of specialization can lead to increased rates of group extirpation. Specialization has little effect on group size but tends to reduce population size and resource abundance. While the two specialization processes produce similar results, cultural specialization can be very much faster. The results are generally consistent with what we know of the formation and maintenance of specialist ecotypes in killer whales, and have implications for the persistence, nature and ecological effects of these apex predators.

Selective reactions to different killer whale call categories in two delphinid species.

The risk of predation is often invoked as an important factor influencing the evolution of social organization in cetaceans, but little direct information is available about how these aquatic mammals respond to predators or other perceived threats. We used controlled playback experiments to examine the behavioral responses of short-finned pilot whales (Globicephala macrorhynchus) off Cape Hatteras, NC, USA, and Risso's dolphins (Grampus griseus) off the coast of Southern California, USA, to the calls of a potential predator, mammal-eating killer whales. We transmitted calls of mammal-eating killer whales, conspecifics and baleen whales to 10 pilot whales and four Risso's dolphins equipped with multi-sensor archival acoustic recording tags (DTAGs). Only playbacks of killer whale calls resulted in significant changes in tagged animal heading. The strong responses observed in both species occurred only following exposure to a subset of killer whale calls, all of which contained multiple non-linear properties. This finding suggests that these structural features of killer whale calls convey information about predatory risk to pilot whales and Risso's dolphins. The observed responses differed between the two species; pilot whales approached the sound source while Risso's dolphins fled following playbacks. These divergent responses likely reflect differences in anti-predator response mediated by the social structure of the two species.

Infanticide in a mammal-eating killer whale population.

Infanticide can be an extreme result of sexual conflict that drives selection in species in which it occurs. It is a rarely observed behaviour but some evidence for its occurrence in cetaceans exists in three species of dolphin. Here we describe observations of an adult male killer whale (Orcinus orca) and his post-reproductive mother killing a neonate belonging to an unrelated female from the same population in the North Pacific. This is the first account of infanticide reported in killer whales and the only case committed jointly by an adult male and his mother outside of humans. Consistent with findings in other social mammals, we suggest that infanticide is a sexually selected behaviour in killer whales that could provide subsequent mating opportunities for the infanticidal male and thereby provide inclusive fitness benefits for his mother.

Imitation of novel conspecific and human speech sounds in the killer whale (Orcinus orca).

Vocal imitation is a hallmark of human spoken language, which, along with other advanced cognitive skills, has fuelled the evolution of human culture. Comparative evidence has revealed that although the ability to copy sounds from conspecifics is mostly uniquely human among primates, a few distantly related taxa of birds and mammals have also independently evolved this capacity. Remarkably, field observations of killer whales have documented the existence of group-differentiated vocal dialects that are often referred to as traditions or cultures and are hypothesized to be acquired non-genetically. Here we use a do-as-I-do paradigm to study the abilities of a killer whale to imitate novel sounds uttered by conspecific (vocal imitative learning) and human models (vocal mimicry). We found that the subject made recognizable copies of all familiar and novel conspecific and human sounds tested and did so relatively quickly (most during the first 10 trials and three in the first attempt). Our results lend support to the hypothesis that the vocal variants observed in natural populations of this species can be socially learned by imitation. The capacity for vocal imitation shown in this study may scaffold the natural vocal traditions of killer whales in the wild.

Killer whale (Orcinus orca) behavioral audiograms.

Killer whales (Orcinus orca) are one of the most cosmopolitan marine mammal species with potential widespread exposure to anthropogenic noise impacts. Previous audiometric data on this species were from two adult females [Szymanski, Bain, Kiehl, Pennington, Wong, and Henry (1999). J. Acoust. Soc. Am. 108, 1322-1326] and one sub-adult male [Hall and Johnson (1972). J. Acoust. Soc. Am. 51, 515-517] with apparent high-frequency hearing loss. All three killer whales had best sensitivity between 15 and 20 kHz, with thresholds lower than any odontocete tested to date, suggesting this species might be particularly sensitive to acoustic disturbance. The current study reports the behavioral audiograms of eight killer whales at two different facilities. Hearing sensitivity was measured from 100 Hz to 160 kHz in killer whales ranging in age from 12 to 52 year. Previously measured low thresholds at 20 kHz were not replicated in any individual. Hearing in the killer whales was generally similar to other delphinids, with lowest threshold (49 dB re 1 µPa) at approximately 34 kHz, good hearing (i.e., within 20 dB of best sensitivity) from 5 to 81 kHz, and low- and high-frequency hearing cutoffs (>100 dB re µPa) of 600 Hz and 114 kHz, respectively.

Evidence for the perceptual origin of right-sided feeding biases in cetaceans.

Foraging behaviour of many cetacean species features the side biases at the population level. The origin of these behavioural lateralisations remains generally unclear. Here we explored lateralisation in aerial display of resident orcas in different behavioural contexts. Side preferences were analysed in lunging during foraging and breaching. One event of each type of displays per individually identified orca was used for analysis. Orcas showed a population-level preference to lunge on the right side when foraging (75% of lunges). In contrast, no lateralisation was found in breaching (54% of breaches to the right, 45% to the left). The right-sided bias in foraging found in orcas is in line with evidence from other whales, both baleen and toothed, and confirms the uniformity of feeding biases among cetaceans. In contrast to breaching, lunging in orcas was associated with fish pursuit, that is, with focused attention to and sensory perception of prey stimulus. The emergence of lateralisation in lunging and the absence of significant bias in breaching suggest that feeding biases in whales are underpinned by sensory lateralisation, that is, by lateralised hemispheric processing of sensory information about the prey. Evidence from orcas may be extrapolated to other cetaceans since right-sided biases in lunging during foraging is a very widespread phenomenon and likely to have a common origin. Our findings support the hypothesis that right-sided feeding biases are determined by left-hemisphere specialisation.

Vocalisations of Killer Whales (Orcinus orca) in the Bremer Canyon, Western Australia.

To date, there has been no dedicated study in Australian waters on the acoustics of killer whales. Hence no information has been published on the sounds produced by killer whales from this region. Here we present the first acoustical analysis of recordings collected off the Western Australian coast. Underwater sounds produced by Australian killer whales were recorded during the months of February and March 2014 and 2015 in the Bremer Canyon in Western Australia. Vocalisations recorded included echolocation clicks, burst-pulse sounds and whistles. A total of 28 hours and 29 minutes were recorded and analysed, with 2376 killer whale calls (whistles and burst-pulse sounds) detected. Recordings of poor quality or signal-to-noise ratio were excluded from analysis, resulting in 142 whistles and burst-pulse vocalisations suitable for analysis and categorisation. These were grouped based on their spectrographic features into nine Bremer Canyon (BC) "call types". The frequency of the fundamental contours of all call types ranged from 600 Hz to 29 kHz. Calls ranged from 0.05 to 11.3 seconds in duration. Biosonar clicks were also recorded, but not studied further. Surface behaviours noted during acoustic recordings were categorised as either travelling or social behaviour. A detailed description of the acoustic characteristics is necessary for species acoustic identification and for the development of passive acoustic tools for population monitoring, including assessments of population status, habitat usage, migration patterns, behaviour and acoustic ecology. This study provides the first quantitative assessment and report on the acoustic features of killer whales vocalisations in Australian waters, and presents an opportunity to further investigate this little-known population.

Ecological knowledge, leadership, and the evolution of menopause in killer whales.

Classic life-history theory predicts that menopause should not occur because there should be no selection for survival after the cessation of reproduction [1]. Yet, human females routinely live 30 years after they have stopped reproducing [2]. Only two other species-killer whales (Orcinus orca) and short-finned pilot whales (Globicephala macrorhynchus) [3, 4]-have comparable postreproductive lifespans. In theory, menopause can evolve via inclusive fitness benefits [5, 6], but the mechanisms by which postreproductive females help their kin remain enigmatic. One hypothesis is that postreproductive females act as repositories of ecological knowledge and thereby buffer kin against environmental hardships [7, 8]. We provide the first test of this hypothesis using a unique long-term dataset on wild resident killer whales. We show three key results. First, postreproductively aged females lead groups during collective movement in salmon foraging grounds. Second, leadership by postreproductively aged females is especially prominent in difficult years when salmon abundance is low. This finding is critical because salmon abundance drives both mortality and reproductive success in resident killer whales [9, 10]. Third, females are more likely to lead their sons than they are to lead their daughters, supporting predictions of recent models [5] of the evolution of menopause based on kinship dynamics. Our results show that postreproductive females may boost the fitness of kin through the transfer of ecological knowledge. The value gained from the wisdom of elders can help explain why female resident killer whales and humans continue to live long after they have stopped reproducing.

Life history evolution: what does a menopausal killer whale do?

Menopause evolved in humans and whales, presumably because older females can help their kin. But how do they help? New research shows that post-menopausal female killer whales lead foraging groups. This leadership is most significant when food is scarce.

Differences in acoustic features of vocalizations produced by killer whales cross-socialized with bottlenose dolphins.

Limited previous evidence suggests that killer whales (Orcinus orca) are capable of vocal production learning. However, vocal contextual learning has not been studied, nor the factors promoting learning. Vocalizations were collected from three killer whales with a history of exposure to bottlenose dolphins (Tursiops truncatus) and compared with data from seven killer whales held with conspecifics and nine bottlenose dolphins. The three whales' repertoires were distinguishable by a higher proportion of click trains and whistles. Time-domain features of click trains were intermediate between those of whales held with conspecifics and dolphins. These differences provided evidence for contextual learning. One killer whale spontaneously learned to produce artificial chirps taught to dolphins; acoustic features fell within the range of inter-individual differences among the dolphins. This whale also produced whistles similar to a stereotyped whistle produced by one dolphin. Thus, results provide further support for vocal production learning and show that killer whales are capable of contextual learning. That killer whales produce similar repertoires when associated with another species suggests substantial vocal plasticity and motivation for vocal conformity with social associates.

Classification of large acoustic datasets using machine learning and crowdsourcing: application to whale calls.

Vocal communication is a primary communication method of killer and pilot whales, and is used for transmitting a broad range of messages and information for short and long distance. The large variation in call types of these species makes it challenging to categorize them. In this study, sounds recorded by audio sensors carried by ten killer whales and eight pilot whales close to the coasts of Norway, Iceland, and the Bahamas were analyzed using computer methods and citizen scientists as part of the Whale FM project. Results show that the computer analysis automatically separated the killer whales into Icelandic and Norwegian whales, and the pilot whales were separated into Norwegian long-finned and Bahamas short-finned pilot whales, showing that at least some whales from these two locations have different acoustic repertoires that can be sensed by the computer analysis. The citizen science analysis was also able to separate the whales to locations by their sounds, but the separation was somewhat less accurate compared to the computer method.

Dose-response relationships for the onset of avoidance of sonar by free-ranging killer whales.

Eight experimentally controlled exposures to 1-2 kHz or 6-7 kHz sonar signals were conducted with four killer whale groups. The source level and proximity of the source were increased during each exposure in order to reveal response thresholds. Detailed inspection of movements during each exposure session revealed sustained changes in speed and travel direction judged to be avoidance responses during six of eight sessions. Following methods developed for Phase-I clinical trials in human medicine, response thresholds ranging from 94 to 164 dB re 1 µPa received sound pressure level (SPL) were fitted to Bayesian dose-response functions. Thresholds did not consistently differ by sonar frequency or whether a group had previously been exposed, with a mean SPL response threshold of 142 ± 15 dB (mean ± s.d.). High levels of between- and within-individual variability were identified, indicating that thresholds depended upon other undefined contextual variables. The dose-response functions indicate that some killer whales started to avoid sonar at received SPL below thresholds assumed by the U.S. Navy. The predicted extent of habitat over which avoidance reactions occur depends upon whether whales responded to proximity or received SPL of the sonar or both, but was large enough to raise concerns about biological consequences to the whales.

Temporal signal processing of dolphin biosonar echoes from salmon prey.

Killer whales project short broadband biosonar clicks. The broadband nature of the clicks provides good temporal resolution of echo highlights and allows for the discriminations of salmon prey. The echoes contain many highlights as the signals reflect off different surfaces and parts of the fish body and swim bladder. The temporal characteristics of echoes from salmon are highly aspect dependent and six temporal parameters were used in a support vector machine to discriminate between species. Results suggest that killer whales can classify salmon based on their echoes and provide some insight as to which features might enable the classification.

Effects of different analysis techniques and recording duty cycles on passive acoustic monitoring of killer whales.

Killer whales in British Columbia are at risk, and little is known about their winter distribution. Passive acoustic monitoring of their year-round habitat is a valuable supplemental method to traditional visual and photographic surveys. However, long-term acoustic studies of odontocetes have some limitations, including the generation of large amounts of data that require highly time-consuming processing. There is a need to develop tools and protocols to maximize the efficiency of such studies. Here, two types of analysis, real-time and long term spectral averages, were compared to assess their performance at detecting killer whale calls in long-term acoustic recordings. In addition, two different duty cycles, 1/3 and 2/3, were tested. Both the use of long term spectral averages and a lower duty cycle resulted in a decrease in call detection and positive pod identification, leading to underestimations of the amount of time the whales were present. The impact of these limitations should be considered in future killer whale acoustic surveys. A compromise between a lower resolution data processing method and a higher duty cycle is suggested for maximum methodological efficiency.

Passive acoustic monitoring of Cook Inlet beluga whales (Delphinapterus leucas).

The endangered beluga whale (Delphinapterus leucas) population in Cook Inlet, AK faces threats from a variety of anthropogenic factors, including coastal development, oil and gas exploration, vessel traffic, and military activities. To address existing gaps in understanding about the occurrence of belugas in Cook Inlet, a project was developed to use passive acoustic monitoring to document the year-round distribution of belugas, as well as killer whales (Orcinus orca), which prey on belugas. Beginning in June 2009, ten moorings were deployed throughout the Inlet and refurbished every two to eight months. Despite challenging conditions consisting of strong tidal currents carrying debris and seasonal ice cover, 83% of mooring deployments were successfully recovered. Noise from water flow, vessel traffic, and/or industrial activities was present at several sites, potentially masking some signals. However, belugas were successfully detected at multiple locations. Detections were relatively common in the upper inlet and less common or absent at middle and lower inlet locations. Killer whale signals were also recorded. Some seasonal variability in the occurrence of both belugas and killer whales was evident.

Experimental evidence for action imitation in killer whales (Orcinus orca).

Comparative experimental studies of imitative learning have focused mainly on primates and birds. However, cetaceans are promising candidates to display imitative learning as they have evolved in socioecological settings that have selected for large brains, complex sociality, and coordinated predatory tactics. Here we tested imitative learning in killer whales, Orcinus orca. We used a 'do-as-other-does' paradigm in which 3 subjects witnessed a conspecific demonstrator's performance that included 15 familiar and 4 novel behaviours. The three subjects (1) learned the copy command signal 'Do that' very quickly, that is, 20 trials on average; (2) copied 100 % of the demonstrator's familiar and novel actions; (3) achieved full matches in the first attempt for 8-13 familiar behaviours (out of 15) and for the 2 novel behaviours (out of 2) in one subject; and (4) took no longer than 8 trials to accurately copy any familiar behaviour, and no longer than 16 trials to copy any novel behaviour. This study provides experimental evidence for body imitation, including production imitation, in killer whales that is comparable to that observed in dolphins tested under similar conditions. These findings suggest that imitative learning may underpin some of the group-specific traditions reported in killer whales in the field.