Discussion 8

Cognitive skills in bottlenose dolphin communication

Vincent M. Janik

Sea Mammal Research Unit, School of Biology, University of St Andrews, Fife KY16 8LB, UK

Forum

Bottlenose dolphins display a behavioural skill set that makes them an interesting model system for the study of complexity in communication and cognition. They are capable of vocal learning, referential labelling, syntax comprehension, and joint attention. In their own com- munication system, these skills are used in individual recognition, group cohesion, and coordination, which suggests that social challenges are a universal selection pressure for complexity in communication and cognition independent of the physical environment.

Animal models in comparative communication studies Mechanisms in animal communication have been studied at a variety of levels, from neurobiology to questions of representation or intention underlying communicative acts. Such studies often draw direct comparisons with human language, placing the degree of complexity of ani- mal communication systems within the context of lan- guage evolution [1,2]. The two best established model systems in this context are nonhuman primates and song birds. Nonhuman primates are an obvious choice when trying to investigate precursors to communication in the human primate, whereas song birds seem suitable due to their vocal learning skills and song syntax. However, both lack significant features of human language that are pres- ent in other animals. Bird song lacks semantics in the sense of utterances referring to objects in the external world [2]. Primates use syntax and reference in their calls, but lack the ability to copy novel sounds [1]. Great apes can learn new gestures and use them in a flexible way that may hint at a gestural origin of human language. However, despite extensive research efforts, scientists have been unable to find a referential use for gestures beyond point- ing in trained, captive animals [1]. It is therefore important to also look further afield for cases that combine vocal learning, syntax, reference, and complex cognitive skills to advance comparative communication studies. Bottle- nose dolphins, Tursiops trunactus and Tursiops aduncus, have long been perceived as fitting these requirements (Figure 1).

The bottlenose dolphin Bottlenose dolphins belong to the delphinid family of the mammalian order cetacea (whales, dolphins, and por- poises). Dolphins are as unlike humans as one can find amongst mammals. Not only do they not possess an oppos- able thumb, but they also lack any kind of limb that could be easily used to manipulate their environment. Their

Corresponding author: Janik, V.M. ([email protected])

home environment is more uniform and less affected by gravity than that of land animals. This allows three- dimensional movement with little restriction, but few to no landmarks are available for orientation. Perhaps not surprisingly, humans also do not share any significant evolutionary history with delphinids since the emergence of the mammalian class. Because dilution effects and the opacity of water limit the usefulness of chemosensory and visual systems, thus removing two important modalities heavily used by most mammals for communication, the dolphin sensory world is primarily acoustic. As a result, dolphins use large repertoires of acoustic signals for com- munication and echolocation [3].

Despite these differences, there are striking similarities between primate and dolphin behaviour. Bottlenose dol- phins live in fission–fusion societies similar to those found in many primate species [4]. Within these societies, males form long-lasting alliances. First-order alliances of two to three animals also form higher order alliances with others when competing with other males. Females have long-last- ing bonds with their offspring and social learning allows dolphins of both sexes to form distinct foraging traditions [4], which results in a kind of niche separation within populations. These features of dolphin society require ad- vanced learning and memory skills and form an ideal arena for the application of social cognition. They also require a finely tuned communication system that allows animals to keep track of individuals and their relationships.

Vocal learning and reference Vocal learning has three distinct forms: production, com- prehension, and usage learning [5], and all three can be found in bottlenose dolphins. Production learning can be used to either make a sound more similar to a model or to create a novel call that is distinctly different from a model. Bottlenose dolphins are able to copy novel sounds at all ages and often produce accurate copies at the first copying attempt [6]. In their own communication system, learning appears to be particularly important in the acquisition of their individually distinctive signature whistles (Figure 2). Learning is used here to develop a novel frequency modu- lation that no other dolphin uses. One strategy to achieve this appears to be selecting a conspecific’s whistle or an- other sound from the environment and modifying it suffi- ciently to make it unique [7]. The invented modulation pattern is an arbitrary signal that carries the identity information that conspecifics recognise even if generated by a computer [8]. Whereas a signature whistle is primarily used by its owner, vocal learning also allows dolphins to learn the whistles used by others and to copy them, effec- tively addressing selected conspecifics [9].

157

TRENDS in Cognitive Sciences

Figure 1. A bottlenose dolphin (Tursiops truncatus) leaping near the river Tay in

Scotland, UK. Bottlenose dolphins show a variety of cognitively advanced

communication skills, such as vocal production learning, syntax comprehension,

and referntial labeling [10].

Forum Trends in Cognitive Sciences April 2013, Vol. 17, No. 4

If an animal invents its own arbitrary and novel signal to broadcast its identity, and other animals copy this signal to address the inventor, one can ask whether signature whistles are referential signals comparable to names or

20

15

10

5

0

kH z 20

15

10

5

0

kH z

20

15

10

5

0

kH z 20

15

10

5

0

kH z

0.5s �me

0.5s �me

0.5s �me

0.5s �me

sex: FEMALE

FB53 born: 1986 sex: FE

sex: MALE

F162 born: 1981 sex: M

Figure 2. Spectrograms of signature whistles of six individual bottlenose dolphins from

picture, identification number, sex, and year of birth of each animal. Each dolphin develo

by copying another individual’s whistle and then modifying it to create a novel and uni

The identity information encoded in the invented modulation pattern is recognised by c

fin photos by Sarasota Dolphin Research Program, taken under National Marine Fisher

158

labels (Box 1). Captive bottlenose dolphins are able to use novel signals to refer to objects that were paired with these signals in training experiments [6]. These signals were then used to ask the animal to report presence and absence of objects, demonstrating that displaced reference is possi- ble [10]. Thus, dolphins clearly can learn to pair whistles with referents. In the wild, signature whistle copying is rare, but, if used, it occurs in response to hearing a known signature whistle [9] or sometimes spontaneously, even in the absence of the corresponding animal [11]. Given their performance in captive experiments, it is difficult to imag- ine that their referential labelling skills would not come into play in signature whistle copying.

Syntax and joint attention Syntax comprehension has been studied extensively in captive bottlenose dolphins. In one study, the animals were taught to associate objects, acts, or modifiers, such as left or right, with signals and learned to respond to strings of such signals. Tests with novel strings of signals demonstrated that they correctly processed the syntactical information in them [10]. No studies have addressed the potential for syntax in wild bottlenose dolphins. However, bottlenose dolphins use a large variety of clicks and pulsed calls that are composed of long sequences of clicks. Given the discrete structure of clicks, there is a large potential for syntactic information in click sequences. Clicks are used in echolo- cation and communication, but only few studies have investigated their communicative function. These studies showed that dolphins are not only able to communicate with clicks [3], but also have a kind of shared or communal perception when one animal is listening to the outgoing and returning clicks produced by an echolocating conspe- cific nearby [12]. This could create a kind of joint attention

20

15

10

5

0

kH z

20

15

10

5

0

kH z

0.5s �me

0.5s �me

MALE

F11 1 born: 1968 sex: FEMALE

FB65 born: 1983

ALE

F188 born: 1996 sex: MALE

F132 born: 1983

TRENDS in Cognitive Sciences

Sarasota Bay, FL, USA. Each panel also shows the corresponding fin identification

ps its own distinctive frequency modulation pattern [3]. Some animals achieve this

que modulation pattern [7]. Others seem to create whistles without using a model.

onspecifics [8] and can be copied to address the inventor of the whistle [9]. Dolphin

ies Service Scientific Research Permits.

Box 1. Reference in animal vocalisations

Reference is important in human language and researchers have

looked extensively for precursors to reference in animal signals.

Reference allows humans to connect concepts, including those

representing objects in the environment, to words [2]. As it is not

possible to access directly how animals represent objects in their

environment cognitively, biologists have used the concept of

functional reference when studying animal signals [14]. To fall in

this category, a signal needs to be structurally discrete, elicited by a

specific stimulus or stimulus class, and the receiver response has to

have little variation between different contexts, including in the

absence of the referent of the call. There are several examples of

food and alarm signals in animals that fulfil these criteria. They are

produced by animals as diverse as bees, chickens, and primates

[14]. At least in the primate examples, individuals need to learn over

time to use and respond to alarm calls in the appropriate context [5].

However, all functionally referential alarm and food calls appear to

be present from birth and consist of signals that cannot be modified

structurally by production learning [5]. There is also no population

variation in the signals’ referents. This lack of flexibility differs from

referential use of signals in humans [2]. However, to look at

reference in learned animal signals, it may be important to look at

other contexts, particularly in the social domain. Several birds, bats,

and delphinids learn group-specific contact calls [5], which can

contain individually-specific features that could be used to refer to

individuals when copied. However, other than anecdotes, there are

surprisingly few reports of this occurring. Aside from the bottlenose

dolphin [3], only some parrots (e.g., the spectacled parrotlet, Forpus

conspicillatus) have been found to label conspecifics in this way.

Here, receivers respond more to calls addressing them than to calls

addressing others [15]. However, it is unclear how stable these

‘labels’ are and who invents them. A wider investigation of whether

learned, individually distinctive features in animal calls are copied

by conspecifics when interacting with or searching for an animal

would be a useful step towards the investigation of precursors to

reference in learned signals.

Forum Trends in Cognitive Sciences April 2013, Vol. 17, No. 4

by default, since the acoustic signals and the echoes show what the click producer is paying attention to. Joint atten- tion has been highlighted as an important component in the evolution of human communication behaviour, empha- sising its role in interactions [13]. It would thus be inter- esting to investigate how much dolphins guide each other’s attention using echolocation.

Concluding remarks These short examples illustrate the complexity underlying bottlenose dolphin communication. Dolphins represent an interesting mixture of close similarities and drastic differ- ences to primates. Cognitively and behaviourally they match many primate features [3,4], whereas their envi- ronment and perceptual worlds are as different as can be imagined. However, even though dolphins are very popular in the public eye, there are relatively few studies on their communication and cognition when compared to primates or birds. One of the main gaps is the absence of theory-of- mind studies on dolphins. Particularly, it is important to

investigate how these animals perform in false belief tasks. This is crucial in order to assess the importance of their capacity for reference in social interactions. In other areas, the direct comparison to human language skills may be less helpful. Dolphins are aquatic mammals that can use sound to explore the environment as well as to share information and attention. They may have evolved other solutions to negotiating their social environment than terrestrial species that divide these tasks between the acoustic and the visual domain. Thus, dolphins may be able to provide insight into the evolution of communicative complexity on a broader scale than if we focus on terrestrial species alone.

Acknowledgements I thank Randall Wells for providing photos and Steve Smart for the production of Figure 2.

References 1 Arbib, M.A. et al. (2008) Primate vocalization, gesture and the

evolution of human language. Curr. Anthropol. 49, 1053–1076 2 Hurford, J.R. (2007) The Origins of Meaning: Language in the Light of

Evolution, Oxford University Press 3 Janik, V.M. (2009) Acoustic communication in delphinids. Adv. Study

Behav. 40, 123–157 4 Connor, R.C. et al. (2000) The bottlenose dolphin: social relationships in

a fission–fusion society. In Cetacean Societies: Field Studies of Dolphins and Whales (Mann, J. et al., eds), pp. 91–126, University of Chicago Press

5 Janik, V.M. and Slater, P.J.B. (2000) The different roles of social learning in vocal communication. Anim. Behav. 60, 1–11

6 Richards, D.G. et al. (1984) Vocal mimicry of computer-generated sounds and vocal labeling of objects by a bottlenosed dolphin, Tursiops truncatus. J. Comp. Psychol. 98, 10–28

7 Fripp, D. et al. (2005) Bottlenose dolphin (Tursiops truncatus) calves appear to model their signature whistles on the signature whistles of community members. Anim. Cogn. 8, 17–26

8 Janik, V.M. et al. (2006) Signature whistle contour shape conveys identity information to bottlenose dolphins. Proc. Natl. Acad. Sci. U.S.A. 103, 8293–8297

9 King, S.L. et al. (2013) Vocal copying of individually distinctive signature whistles in bottlenose dolphins. Proc. R. Soc. B: Biol. Sci. 280, 20130053

10 Herman, L.M. (2006) Intelligence and rational behaviour in the bottlenosed dolphin. In Rational Animals? (Hurley, S. and Nudds, M., eds), pp. 439–467, Oxford University Press

11 Watwood, S.L. et al. (2005) Signature whistle use by temporarily restrained and free-swimming bottlenose dolphins, Tursiops truncatus. Anim. Behav. 69, 1373–1386

12 Xitco, M.J. and Roitblat, H.L. (1996) Object recognition through eavesdropping: passive echolocation in bottlenose dolphins. Anim. Learn. Behav. 24, 355–365

13 Tomasello, M. et al. (2005) Understanding and sharing intentions: the origins of cultural cognition. Behav. Brain Sci. 28, 675–691

14 Evans, C.S. (1997) Referential signals. Perspect. Ethol. 12, 99–143 15 Wanker, R. et al. (2005) Vocal labelling of family members in spectacled

parrotlets, Forpus conspicillatus. Anim. Behav. 70, 111–118

1364-6613/$ – see front matter � 2013 Published by Elsevier Ltd.

http://dx.doi.org/10.1016/j.tics.2013.02.005 Trends in Cognitive Sciences, April 2013,

Vol. 17, No. 4

159