The Use of Referential Gestures in Ravens in the Wild

8/18/2019 The Use of Referential Gestures in Ravens in the Wild

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NATURE COMMUNICATIONS | 2:560 | DOI: 10.1038/ncomms1567 | www.nature.com/naturecommunications

© 2011 Macmillan Publishers Limited All rights reserved

Received 5 Aug 2011 | Accepted 26 Oct 2011 | Published 29 Nov 2011 DOI: 10.1038/ncomms1567

Around the age of one year, human children start to use gestures to coordinate attentiontowards a social partner and an object of mutual interest. These referential gestures have been

suggested as the foundation to engage in language, and have so far only been observed in great

apes. Virtually nothing is known about comparable skills in non-primate species. Here we record

thirty-eight social interactions between seven raven (Corvus corax) dyads in the Northern Alps,

Austria during three consecutive field seasons. All observed behaviours included the showing

and/or offering of non-edible items (for example, moss, twigs) to recipients, leading to frequent

orientation of receivers to the object and the signallers and subsequent affiliative interactions.

We report evidence that the use of declarative gestures is not restricted to the primate lineage

and that these gestures may function as ‘testing-signals’ to evaluate the interest of a potential

partner or to strengthen an already existing bond.

1 Max Planck Institute for Ornithology, Research Group ‘Comparative Gestural Signalling’, Eberhard-Gwinner-Straße, Geesehouse, 82319 Seewiesen,

Germany. 2 Department of Cognitive Biology, University of Vienna, 1010 Vienna, Austria. Correspondence and requests for materials should be addressed

to S.P. (email: [email protected]).

The use of referential gestures in ravens

(Corvus corax) in the wild

Simone Pika1 & Thomas Bugnyar2


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NATURE COMMUNICATIONS | DOI: 10.1038/ncomms1567



From early childhood on, human inants requently use dis-tinct gestures such as showing, offering, giving (or example,ood, objects), and pointing1 to coordinate attention towards a

social partner and an object o mutual interest2. Tese triadic inter-actions qualiy as reerential because they are used to attract theattention o others to some outside entity, are mechanically ine-ective and include joint-attention behaviours (or example, eye-contact with an adult beore, during or aer the perormance o agesture). Tey are used either to make requests (imperatives, or

example, ‘take this’) or to show a third entity to recipients, withoutrequiring the person to do anything else but to attend to the object(declaratives, or example, ‘look at this’)3. Tese gestures thusmark a pivotal change in the inant’s communicative competenceand have been viewed as the oundation to engage in symbolicallymediated conversations1,4.

In stark contrast, observations o comparable gestures in ourclosest living relatives, the great apes, are relatively rare and mainlyconcern captive and/or human-raised individuals5–10. Te mostcompelling evidence o reerential gestures in natural environmentsso ar stems rom chimpanzees at the Ngogo community, Uganda,who use so-called directed scratches, to indicate distinct spots ontheir bodies to be groomed11. Tese attention-getters represent, dueto their two-tiered intentional structure (combining social intention

to get something done and the ‘reerential’ intention to draw theattention o the recipient to some third entity), an extremely rareorm o communication evolutionarily and have been suggested asconfined to primates only 12.

However, are such sophisticated gestures truly unique to theprimate lineage?

In the present study, we aimed to address this question by inves-tigating the use and underlying cognitive complexity o distinctnonvocal signals in ravens (Corvus corax ) in their natural environ-ment. Ravens are songbirds, which show a relatively high degree osong learning, including the ability to mimic the songs o other birdsand human speech, along with environmental sounds13,14. AlthoughGwinner14 in the middle o the last century, already emphasizedtheir gestural plasticity and flexibility, research into this communi-

cative domain is virtually nonexistent.Ravens belong to the corvid amily, which is renowned orexceeding the majority o other avian species with the exception osome parrots,15,16 and rivalling even primates in many physical andsocial cognitive domains (or example, see res 17,18 and 19). Unlikenonhuman primates, but similarly to humans, corvids rely heavilyon cooperation between pair-partners14,20. Ravens in particular canbe characterized by ontogenetically shaped intra-pair communica-tion14,20,21, relatively long-time periods to orm pairs14,20,22, and varia-tion in relationship quality within non-breeder groups23. Moreover,ravens oen use non-ood items in social interactions20,24. Te motivesto orm and maintain affiliate relationships may, thus, have been

crucial in boosting not only their cognitive but also, especially, their vocal and nonvocal communicative abilities. Notably, first stages osocial bonding may involve behaviours to direct other’s attentiontriadically and reerentially 25.

Our results provide evidence that the use o reerential gesturesis not restricted to the primate lineage. Ravens also use distinctobject-oriented behaviours to mainly direct conspecific’s attentionto a third entity triadically and reerentially. As the majority o ges-tures were used in mixed-sex dyads, these gestures seem to unc-

tion as ‘testing-signals’ to evaluate the interest o a given partneror to strengthen an already existing bond. Our results thus sup-port the hypothesis that evolutionary new inerential processesensue when communication becomes governed by more coopera-tive motives26, and that examples o convergent evolution in dis-tant-related species provide crucial clues to unravel the mystery olanguage origins.

ResultsGesture use. We recorded 38 social interactions o 7 raven dyads intheir natural habitat (able 1). Eight o twelve possible interactantswere tagged and could clearly be identified. Four individuals wereuntagged and, based on their morphology and behaviour, couldonly be clustered in relation to their age, but not sex class. Te our

dyads, which consisted o tagged individuals consisted all o mixed-sex pairs. All dyads engaged in two distinct behaviours, showingand offering. wenty-five instances consisted o showing, definedas ‘picking up a non-ood item (or example, moss, small stones, ortwigs), holding it up in the beak, head straight or tilted upwards, andstaying in this position (Fig. 1)’. en instances consisted o offering,

Figure 1 | Showing. Raven showing an object to conspecifics.

Table 1 | Individuals, age, recipients, behavioural parameters.

Signaller(1=male;2=female)

Year ofbirth

Recipient(1=male;2=female)

Year ofbirth

Showing Offering Undecided Average useof behaviour/observation

bout

Change fromshowing to

offering

CA [1] 2008 UI [?] ~2007/8 1 3 0 1 0

KL [1] 2008 TI [2] 2006 3 5 0 1.6 0

OR [2] 2009 PO [1] 2009 2 0 2 1 1

PO [1] 2009 OR [2] 2009 6 2 1 2.25 0

SH [1] 2008 UI [?] ~2007/8 3 0 0 1 0

TR [2] 2008 CA [1] 2008 2 0 0 2 0

UI [?] ~2007/8 UI [?] ~2007/8 8 0 0 8 0

Total — — — 25 10 3 — 1

Individuals identified by two-letter codes. The two letter code UI indicates an untagged individual with only estimated year of birth.

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DiscussionTe present study aimed to investigate whether members o the corvid amily, ravens, use nonvocal signals as sophisticated, reerentialmeans.

Our results showed that ravens used distinct object-orientedbehaviours, showing and offering, to already attending recipientso the opposite sex. In response to these behaviours, recipientsoriented themselves most oen directly towards the object andthe signaller and engaged, subsequently, more oen in affiliativebehaviour with the signaller (including behaviours such as bill-ing and manipulating o the object) than in agonistic or deensivebehaviour.

Tree hypotheses may account or these observations. First,showing and offering may not serve a communicative unction, butmay be due to the predisposition o especially young individuals toexplore and manipulate almost every kind o object they encounter28.It has been suggested that the manipulation and exploration oobjects may serve to amiliarize young ravens with potential ooditems that may be unique to their ecological circumstances28. Fur-thermore, ravens like other ood-storing corvids devote mucho their time to cache ood in temporary storages29. Tey are alsoknown or caching small non-ood items30, suggesting that they‘enjoy’ hiding items and, in the absence o ood, become directedtowards objects. Tis hypothesis suggests that showing and offer-ing takes place irrespectively o the presence and attentional stateo a given recipient. Tese two predictions do not accord with our

observations (Figs 1 and 2).Second, showing and offering may not represent communica-tive signals but are simply due to the intrinsic motivation31 to shareood20. Contrary to nonhuman primates, active giving or alloeed-ing is very common in birds, especially with regard to parent–off-spring32 and courtship eeding33,34. Tis motivation may be so strongthat the birds perorm the behaviour even i no ood is available.I this hypothesis was true, then we would expect that ravensonly offer, but not show objects, to recipients and that all interac-tions end in attempts to alloeed the recipient. However, we onlyobserved once that a raven that had offered a piece o moss to arecipient, tried to subsequently put it in the beak o the recipient.In addition, we did not observe any other characteristic behaviourssuch as twitching o the wings and eeding vocalizations, whichhave been described to accompany alloeeding14,20.

0

20

40

60

80

100

120

A v e r a g e f r e q u e n c y i n %

Attending Not attending

Figure 2 | Adjustment to audience effects. Average use (in %) of showing

and offering (collapsed) to an attending and non-attending recipient. Error

bars indicate the s.d.

defined as ‘picking up a non-ood item (or example, moss, smallstones, or twigs), holding it up in the beak and moving the headup- and/or downwards repeatedly’ (able 1).

In the majority o the observed cases, these behaviours weredirected to a recipient (100%), were mechanically ineffective (thatis, they were not designed to act as direct physical agents, contraryto behaviours such as sticking an object in the beak o a given recipi-ent) (95%), and received a voluntary response (100%). Concerningthe underlying cognitive complexity 27, the analyses showed that thebehaviours were ollowed by response waiting (100%), and were,significantly, more oen directed to an attending recipient than toa non-attending recipient (Wilcoxon test: Z = − 2.371, n = 7, exactP -value = 0.018; Fig. 2).

Orientation of recipients and subsequent behaviour of dyad.In addition, aer the perormance o a signal recipients orientedthemselves significantly more oen towards the signaller and theobject than away rom them (Wilcoxon test: Z = − 2.375, n = 7,exact P -value = 0.018; Fig. 3). In the majority o cases, recipientsengaged subsequently in affiliative interactions with the signaller(approaching, billing, pretend-eeding, manipulating o the objecttogether: 77%), and only rarely in agonistic/deensive (4%) ormore neutral interactions (other behaviour: vocalizing, ignoring:11%; change o attentional state rom non-looking to looking: 8%).Tese differences were significant or affiliative versus agonistic/deensive behaviour (Friedman X 3

2 = 15.879, P = 0.001; Wilcoxontest: Z = − 2.375, n = 7, post-hoc corrected P -value (Holm) = 0.036;Fig. 4).

0

20

40

60

80

100

120

A v e r a g e f r e

q u e n c y i n %

Orientate toward Orientate away

Figure 3 | Orientation of the recipient after performance of showing

and offering. Average orientation of the recipient (in %) towards and

away from the signaller after the performance of showing and offering

(collapsed). Error bars indicate the s.d.

0

20

40

60

80

100

120

A v e r a g e f r e q u e n c y i n %

Subsequent behaviour

Affiliative

Defensive/agonistic

Change of attentional state

Other behavior

Figure 4 | Subsequent behaviour in dyads after performance of showing

and offering. Average frequency (in %) of either affiliative (approaching,

billing, manipulating the object together), defensive/agonistic behaviour

(defensive posture, leave, flee, attack), attentional state changes (from

non-looking to looking) or other behaviour (vocalizing, ignoring) between

members of the dyad after the performance of showing and offering

(collapsed). Error bars indicate the s.d.

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Tird, showing and offering may be used communicativelyto direct others’ attention intentionally to external things triadi-cally and reerentially. Consistent with this hypothesis is that bothbehaviours were always directed to a recipient, were mechanicallyineffective, received a voluntary response, and showed goal-direct-edness and sensitivity to the attentional state o recipients. Tesesignals thus qualiy, ollowing the criteria o Bates and colleagues3 and Pika27 as intentionally produced communicative gestures andare understood by receivers. Our observations thus strengthen the

findings o Gwinner14, who suggested a high degree o flexibilityin ravens’ nonvocal signalling. Interestingly, the only other studysuggesting reerential gestural abilities in birds, concerns anotherhighly social and cooperative songbird belonging to the amily othe Artamidae35. Kaplan36 reported that Australian magpies (Gym-norhina tibicen) show a distinct body posture when encounteringa sheltered or partly hidden aerial raptor, the wedge-tailed eagle( Aquila audax ): they lean orward in an angle o nearly 45° belowa normal resting position, while the body is orming a straight linewith the beak acing the eagle. Because additionally arriving Aus-tralian magpies engaged in gaze ollowing, when landing and quiteoen also adopted the same posture, Kaplan argued that this behav-iour qualifies as a proto-declarative act o ‘pointing’ to change thestate o knowledge o another conspecific (or a critical evaluation

o the use o the term proto-declarative or non-linguistic species,res 5, 37). However, as the majority o arriving magpies adopt thesame posture, the signal might, in act, be aimed at the predatoritsel rather than serving to inorm conspecifics38,39. Further researchis needed to investigate whether Australian magpies and otherhighly social and cooperative bird species use nonvocal signals asintentionally produced strategies to inorm conspecifics about thirdentities and/or events.

In sum, our results provide the first evidence that ravens, simi-larly to pre-linguistic human children and great apes, use nonvocalsignals to direct the attention o conspecifics to outside entities triad-ically and reerentially (or ravens’ unctional reerential vocal abili-ties, re. 40). However, contrary to chimpanzees, whose reerentialgestures to conspecifics are requests or distinct activities (or exam-

ple, ‘groom me here’) and are directed to partners o both sexes11,41

,ravens’ reerential gestures seem mainly be perormed towardsmembers o the opposite sex and may thus unction as ‘test signals’.As ravens rely heavily on cooperation between pair-partners to raisetheir young and bond or lie20, they invest in relatively long timeperiods to find and choose the right partner. Gestures such as show-ing and offering might thus have developed in this object-orientedspecies, to explore whether a given partner would be interested inattending to onesel and a given object o interest; and/or to test andstrengthen an already existing relationship. Te unction o thesegestures may, thus, be very similar to declarative gestures (used toshare attention or to comment on things) o pre-linguistic humanchildren such as pointing and showing, which are most requentlyused between individuals with already existing strong bonds (or

example, mother–inant) or in situations o uncertainty, in whichbonds just have to be ormed (or example, meeting o strangers)25.Te use o triadic reerential signals in wild ravens thus adds to

the growing evidence that corvids are in many cognitive domainscomparable to nonhuman primates and may even exceed them insome42,43. Furthermore, because ravens, like humans, rely heavilyon cooperation between pair-partners20, our results strengthen thehypothesis that evolutionary new inerential processes ensue whencommunication becomes governed by more cooperative motives 26.o reconstruct hominid evolution and the changes that paved theway or language to evolve, we thus have to view the likely adapta-tions o early hominins generally, rather than with specific reerenceto living chimpanzees only 44. Detailed insight in communicativeabilities o our closest phylogenetic relatives, the nonhuman pri-mates, can, by both homology and analogy, help in reconstructing

the behaviour o the last common ancestor o Pan and Homo and,perhaps, some aspect o early hominin behaviour. Examples o convergent evolution in distant-related species, however, will providecrucial clues to the types o problems that particular morphologicalor behavioural mechanisms were ‘designed’ to solve45.

MethodsData collection. We observed individually marked members (able 1) o a wildraven community in Northern Alps, Austria, which are habituated to human

observers at oraging and socializing sites within areas o the Cumberland Wild-park, Grünau. Observations were carried out on 68 days, outside the breedingseason during three consecutive field periods (September 2008, June–August 2009and June 2010). Communicative behaviour was recorded on an opportunistic basis(sampling rule: behaviour sampling; recording rule: continuous recording, Martin& Bateson, 1994), using a HD-camera (Sony HDR-CX11E HD Camcorder) and aPersonal digital assistant.

Gestural definition. Following the primate literature27, gestures were defined asmovements o the limbs or head and body that are directed towards a recipient,are goal-directed, mechanically ineffective (that is, they are not designed to act asdirect physical agents) and receive a voluntary response. Te ollowing behaviouralcriteria were used to iner goal-directedness: gazing at the recipient, and responsewaiting (the signaller waits or a response aer the signal has been produced).

Data coding, reliability and statistical analyses. Te digital videotapes weretranserred to a computer and cut into salient segments. Te data collected with the

Personal digital assistant were also transerred to a computer. All data were codedusing the program Adobe Premiere 7 and/or Excel. en percent o the data set wascoded or accuracy by a second observer, resulting in a Cohen’s Kappa o 0.82, anexcellent level o agreement46. Non-parametrical tests were applied to carry outstatistical analyses, ollowed by post-hoc-tests or several pairwise-comparisons(Holms).

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AcknowledgementsTis paper is dedicated to the memory o Christine Elisabeth Klein. We are grateul

to the late Eberhard Gwinner or inspiring this work. We thank Andrea Schell, ina

Fromme and the whole team o the KLF in Grünau or invaluable assistance in the

field and or helpul discussion. For comments on earlier dras and discussion, we

thank obias Deschner, Chris Knight, Wolgang Wickler and Jochen Wol. Tis project

was supported by a seed-corn und o the Royal Society (RMS Re: 54550) and a Sofa

Kovalevskaja Award o the Alexander von Humboldt Foundation to S.P. and a SAR

program (Y366-B17) o the Austrian Science Fund (FWF) to .B.

Author contributionsS.P. and .B. designed the study, and wrote the paper. S.P. collected the majority o data

and analysed the data.

Additional informationCompeting financial interests: Te authors declare no competing financial interests.

Reprints and permission inormation is available online at http://npg.nature.com/

reprintsandpermissions/

How to cite this article: Pika, S. & Bugnyar, . Te use o reerential gestures in ravens

(Corvus corax ) in the wild. Nat. Commun. 2:560 doi: 10.1038/ncomms1567 (2011).


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