Black-capped chickadees (Poecile atricapillus) discriminate between naturally-ordered and scramble-ordered chick-a-dee calls and individual preference is related to rate of learning

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Highlights

  • Black-capped chickadee chick-a-dee calls are delivered in a fixed order.

  • Black-capped chickadees respond at reduced rates to scrambled calls in the field.

  • Black-capped chickadees also responded differentially to scrambled calls in the lab.

  • Black-capped chickadees treated normal and scrambled calls as distinct categories.

Abstract

Though many forms of animal communication are not reliant on the order in which components of signals are combined to be effective, there is evidence that order does matter for some communication systems. In the light of differential responding to calls of varying note-order observed in black-capped chickadees in the field, we set out to determine whether chickadees recognize syntactically-ordered and incorrectly-ordered chick-a-dee calls as separate and distinct conceptual categories using both an auditory preference task and go/no-go operant conditioning paradigm. Results show that chickadees spent more time on the perch that did not produce sound (i.e., silent perch) than on either of the acoustic perches (i.e., natural and scrambled order chick-a-dee call playback) and visited the perch associated with naturally-ordered calls more often than the perch associated with scrambled-order calls. Birds in both the True natural- and scrambled-order call groups continued to respond according to the contingencies that they learned in Discrimination training, indicating that black-capped chickadees are capable of perceiving and acting upon the categories of natural- versus scrambled-ordered calls.

Introduction

Most forms of animal communication are thought to be non-syntactic, meaning that unique signals are employed to serve different purposes in various situations (Nowak et al., 2000). For example, vervet monkeys (Cercopithecus aethiops) and Japanese tits (Parus minor) produce distinct alarm vocalizations in response to avian versus terrestrial predators (Seyfarth et al., 1980, Suzuki and Ueda, 2013). In contrast, syntactic communication, as is seen in human language, involves individual components of a signal having their own meaning and the combination of those components producing different and varied meanings (Nowak et al., 2000). A major hurdle of understanding the origins of human language is determining how human language could have evolved from non-human animal communication through the process of natural selection (Suzuki et al., 2018). This endeavor is made more difficult by the fact that our closest evolutionary relatives, the great apes, do not possess syntactic communication systems (Fitch, 2010). Researchers have had to look more distantly to find species that share some of the traits involved in human language.

Many nonhuman animal species vocal communication putatively follow rules of syntax in their vocalizations. For example, non-human primates, humpback whales, and songbirds have all been shown to produce vocalizations that follow syntactical rules to different degrees (see Zuberbühler, 2019 for an extensive recent discussion of this topic). Specifically, Diana monkeys (Cercopithecus diana; Candiotti et al., 2012) alter the ordering of their vocalizations in a contextually-dependent manner, with different combinations being used during either positive or negative social interactions. Similarly, Campbell’s monkey (Cercopithecus campbelli) alarm calls are delivered with different syllable order depending on the urgency of the situation (Ouattara et al., 2009). In addition to nonhuman primates, several bird species are also sensitive to syntactical rules contained in their vocalizations. The Japanese great tit (Parus minor) have been shown to behave differently when they are exposed to different note types or different orders of call notes (Suzuki et al., 2016) and they are not the only members of the Parid family that follow syntactical rules in the perception or production of their species-specific vocalizations. Hailman and Ficken (1986) noted that the chick-a-dee call of black-capped chickadees (Poecile atricapillus), a small species of North American songbird, possesses a computable syntax not unlike that of human language. Chick-a-dee calls consist of four main note types that are amalgamated following a fixed order (A → B → C → D) though individual note types can be repeated or omitted, yielding a theoretically unlimited repertoire of producible call types (Hailman et al., 1985). Chickadees can use their chick-a-dee call as a mobbing call, warning and recruiting both con- and heterospecifics of the presence of predators (Hurd, 1996). The composition of the call changes depending on how dangerous the predator is perceived to be: chick-a-dee calls with more D notes are produced to higher threat owls and hawks compared to low threat predators (Templeton et al., 2005). In a mobbing situation, the same vocalization type can thus convey different meanings depending on the number and type of notes produced. In addition to threat-level cues, the chick-a-dee call also contains information about species identity (Bloomfield and Sturdy, 2008, Bloomfield et al., 2005), flock membership (Mammen and Nowicki, 1981, Nowicki, 1989), and individual identity (Charrier et al., 2004) and birds in the field have been shown to be sensitive to the order of notes within calls, showing reduced responding to playback of calls with reversed syntax (Charrier and Sturdy, 2005).

In the light of differential responding to calls of varying composition observed in black-capped chickadees in the field, we set out to determine whether black-capped chickadees recognize syntactically-ordered and incorrectly-ordered chick-a-dee calls as separate and distinct conceptual categories. Specifically, we investigated the order of notes in the call in two stages. In the first stage of the current study, we designed a behavioral choice preference task to investigate if chickadees demonstrated a preference for correctly-ordered chick-a-dee calls over incorrectly-ordered (i.e., scrambled) chick-a-dee calls. In the second stage of the experiment, we designed an operant conditioning discrimination task to determine if black-capped chickadees perceive natural-ordered chick-a-dee calls as a separate perceptual category from scrambled-ordered chick-a-dee calls. We also tested whether there was a relationship between preference in stage one and performance in stage two.

The results of this study will strengthen our knowledge of the perception of structure and meaning of black-capped chickadee chick-a-dee calls and, more broadly, will add to our understanding of how syntactic communication systems may differ from non-syntactic systems in important ways. First, in study one, the choice-based preference task is designed to allow us to test which call order a bird chooses to hear, and not only whether birds respond with increased vocalizations or approach to particular vocalizations as in previous playback studies. Second, in experiment two, the operant discrimination study is designed to allow us to test for the particular perceptual and cognitive mechanisms that birds are tapping into to perceive natural versus altered-syntax vocalizations. Additionally, the interaction of both order preference and performance in the discrimination task will allow us to determine if birds are able to learn the discrimination better when reinforced for preferred versus not-preferred categories. Taken together, the results of these studies will expand our understanding of syntax usage in black-capped chickadees specifically and in nonhuman animals more generally.

Section snippets

Subjects

Twenty black-capped chickadees (9 males, 11 females) were tested between July 17, 2017 and March 9, 2018. Birds were captured in Edmonton, Alberta, Canada (North Saskatchewan River Valley, 53.53°N, 113.53°W; Mill Creek Ravine, 53.52°N, 113.47°W) between February 5, 2015 and February 6, 2017. Birds were determined to be at least one year of age at time of capture by examining the shape and color of outer tail retrices (Pyle, 1997) and sex was determined by DNA analysis of blood samples (

Response to perches

Fig. 2 shows the average amount of time spent on each of the three perches and Fig. 3 shows the average number of visits to each of the three perches. We conducted a repeated measures ANOVA where the average amount of time on each of the three perches (e.g., natural order, scrambled order, silence) was the within-subjects factor and sex was the between-subjects factor. Mauchly’s test indicated that the assumption of sphericity had not been violated, χ2(2) = 3.094, p = .213. There was a

Discussion

In a series of two experiments, both a playback experiment where birds could request the playback stimuli, and an operant conditioning experiment, we examined the preference for and perceptual mechanisms underlying, naturally-ordered and scrambled chick-a-dee calls in black-capped chickadees. In this manner, we could evaluate the relationship between individual preference and discrimination performance as it pertains to natural- and unnaturally-ordered conspecific calls. We first conducted a

Conclusions

In the present study, we used two behavioral tasks to evaluate the relationship between preference for and ability to discriminate between natural- and scrambled-order chick-a-dee calls. Our results indicate that, not only do chickadees display individual preference for one type of call over the other, and interestingly a preference for silence over any playback, the magnitude and direction of their preference influences the rate at which they learn to discriminate between the two types of

Acknowledgements

All animal studies were conducted in accordance with the Canadian Council on Animal Care guidelines and policies and with approval from the Animal Care and Use Committee for Biosciences for the University of Alberta. Chickadees were captured and research was carried out under an Environment Canada Canadian Wildlife Service Scientific permit, Alberta Fish and Wildlife Capture and Research permits, and a City of Edmonton Parks Permit. This research was supported by a Natural Sciences and

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