Joint attention skills in wild Arabian babblers (Turdoides squamiceps): a consequence of cooperative breeding?

Yitzchak Ben Mocha et al. Joint attention skills in wild Arabian babblers (Turdoides squamiceps): a consequence of cooperative breeding?, Proceedings of the Royal Society B: Biological Sciences (2019). Apr 3 2019. DOI: 10.1098/rspb.2019.0147

Abstract

Human cooperation strongly relies on the ability of interlocutors to coordinate each other's attentional state: joint attention. One predominant hypothesis postulates that this hallmark of the unique cognitive system of humans evolved due to the combination of an ape-like cognitive system and the prosocial motives that facilitate cooperative breeding. Here, we tested this hypothesis by investigating communicative interactions of a cooperatively breeding bird species, the Arabian babbler (Turdoides squamiceps). The behaviour of 12 wild social groups was observed focusing on two distinct communicative behaviours: object presentation and babbler walk. The results showed that both behaviours fulfilled the criteria for first-order intentional communication and involved co-orientation of recipients' attention. In turn, recipients responded with cooperative and communicative acts that resulted in coordinated joint travel between interlocutors. These findings provide the first evidence that another animal species shows several key criteria traditionally used to infer joint attention in prelinguistic human infants. Furthermore, they emphasize the influence of cooperative breeding on sophisticated socio-cognitive performances, while questioning the necessity of an ape-like cognitive system underlying joint attentional behaviour.

1. Introduction

The extraordinary degree of cooperation exhibited by humans seems unrivalled in the animal kingdom [1,2]. Theorists have implicated a specific cognitive capacity, joint attention, as one of the essential building blocks for the evolution of the cooperative abilities of humans [1,3]. Traditionally, joint attention has been defined as the ability to attract and coordinate the attention of a recipient towards a locus of mutual interest (e.g. an object/event in the environment [4]). Precursors of this cognitive capacity can already be found in human infants at the age of approximately six months, who respond to joint attention by following the direction of a caretaker's gesture [5]. At the age of 9–12 months, infants are capable of initiating joint attention with a social partner by gesturing towards a locus of mutual interest [4]. Consequently, the development of joint attention skills is seen as a fundamental milestone in the ontogeny of human cooperative communication [5,6]. Some scholars even see joint attention as the ‘small difference that made a big difference’ in the cognitive evolution of our species [3].

One predominant hypothesis about the evolution of human sophisticated social cognition, the ‘cooperative breeding’ hypothesis [2], postulates that cooperative breeding installed prosocial psychological functioning supporting systematic alloparental care. This, in turn, resulted in immediate consequences for socio-cognitive performance [7]: Caretakers of cooperative breeders evolved specific cognitive capacities for understanding the needs of others' offspring. In parallel, the offspring developed elaborate communicative signalling to attract attention and care from caretakers other than their mothers [8]. Concerning humans, it has been argued that the exceptional co-occurrence of an existing ape-like cognitive system together with humans’ systematic reliance on alloparental care [9,10] gave rise to unique socio-cognitive capacities such as joint attention (figure 1) [2,7].

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However, are joint attentional skills indeed uniquely human and is the combination of an ape-like cognitive system and cooperative breeding a crucial prerequisite?

To date, relatively little is known about joint attentional skills and the acting selection pressures in other animal species. Furthermore, whether specific behaviours of non-human animals towards human caretakers (e.g. gaze alternation in chimpanzees, Pan troglodytes [11]; pointing in bottlenose dolphins, Tursiops truncatus [12]; and vocal learning in grey parrots, Psittacus erithacus [13]) qualify as joint attentional skills in the human sense is subject to a contentious debate [3,14,15].

Here, we revisited the claim that joint attentional skills are a uniquely human ability [3,15] and tested whether the combination of an ape-like cognitive system and cooperative breeding represents a necessary requirement for joint attention to unfold [2]. We predicted that if an ape-like cognitive system and cooperative breeding are both necessary for joint attention [2,7], bird species will not exhibit key hallmarks of this trait. However, if an ape-like cognitive system is not necessary, but cooperative breeding does facilitate the performance of joint attention skills [16], cooperatively breeding species will demonstrate hallmarks of joint attention. To test these predictions, we investigated communicative interactions in a cooperatively breeding bird species, the Arabian babbler (Turdoides squamiceps), in the wild.

Arabian babblers live in stable social groups [17], consisting of 2–20 kin and non-kin from both sexes [17]. All members provide substantial allopaternal care and use elaborate communicative signalling [17]. We focused on two distinct signals, ‘object presentation’ [18] and ‘babbler walk’, which are frequently used to solicit following behaviour from conspecifics. object presentation involves the discreet presentation of an object to attract the recipient's attention without being seen by other group members. The goal is to lead the recipient towards a hidden location for copulation [18] (see electronic supplementary material, video S1). babbler walk is a multi-modal signal that involves conspicuous wing waving and vocalizations, and is used to solicit a conspecific to follow the signaller (figure 2).

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We paid special attention to two distinct issues that have hampered comparative research on joint attention. First, disagreement on an applicable definition of joint attention has so far prevented valid quantitative comparisons between human and other animal species [19–21]. For example, some define joint attention as the ‘intentional co-orientation of two or more organisms to the same locus’ [21]. Others (e.g. [3]), by contrast, require complex mind reading and define it as ‘the mutual awareness of having attended to the same entity between two (or more) individuals. Mutual awareness is established through communication by at least one individual during mutual gaze’ [20]. To overcome this lack of consensus, we refrained from testing whether communicative episodes between Arabian babblers fit a specific definition. Instead, we investigated whether communicative interactions that were initiated by object presentation and babbler walk fulfilled distinct hallmarks that have traditionally been used to infer joint attention in prelinguistic human infants: (i) intentional communication (e.g. [21,22]), (ii) co-orientation of attention (e.g. [4,15]) and (iii) mutual awareness (e.g. [20,23]). By applying this approach, we aimed to instigate a constructive discussion on joint attentional skills that provides useful tools to pinpoint the different degrees of joint attention and cognitive capacities involved [19].

Second, research on joint attention in non-human species has been strongly biased towards interactions with objects (e.g. [12,20]). However, joint attention can revolve around any type of locus [15] such as, for instance, the interlocutors themselves, or the activity they are performing at the time [4,24]. Hence, we examined whether signallers acted to attract and co-orient recipients' attention to their joint travel.

We thus investigated whether communicative episodes initiated by object presentation and babbler walk fulfil the following three key hallmarks of joint attention (see table 1 and methods for detailed operational criteria).


Check also Yitzchak Ben Mocha et al. Intentional Presentation of Objects in Cooperatively Breeding Arabian Babblers (Turdoides squamiceps), Frontiers in Ecology and Evolution (2019). DOI: 10.3389/fevo.2019.00087

Popular: Attention skills in a nonhuman cooperative breeding species. Max Planck Society Press Article, Apr 11 2019. https://phys.org/news/2019-04-attention-skills-nonhuman-cooperative-species.html