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.

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.

The Future of Artificial Intelligence in Monitoring Animal Identification, Health, and Behaviour.

With many advancements, technologies are now capable of recording non-human animals' location, heart rate, and movement, often using a device that is physically attached to the monitored animals. However, to our knowledge, there is currently no technology that is able to do this unobtrusively and non-invasively. Here, we review the history of technology for use with animals, recent technological advancements, current limitations, and a brief introduction to our proposed novel software. Canadian tech mogul EAIGLE Inc. has developed an artificial intelligence (AI) software solution capable of determining where people and assets are within public places or attractions for operational intelligence, security, and health and safety applications. The solution also monitors individual temperatures to reduce the potential spread of COVID-19. This technology has been adapted for use at the Toronto Zoo, initiated with a focus on Sumatran orangutans (Pongo abelii) given the close physical similarity between orangutans and humans as great ape species. This technology will be capable of mass data collection, individual identification, pose estimation, behaviour monitoring and tracking orangutans' locations, in real time on a 24/7 basis, benefitting both zookeepers and researchers looking to review this information.

Can you hear me now? The effect of signal degradation on perceived predator threat in black-capped chickadees (Poecile atricapillus).

Avian predators vary in their degree-of-threat to chickadees; for example, smaller owls and hawks are of higher threat to chickadees as they can easily maneuver through the trees, while larger predators cannot. We conducted an operant go/no-go discrimination task to investigate the effect of signal degradation on perceived threat. Chickadees were trained to respond to high-threat northern saw-whet owl (NSWO) or low-threat great horned owl (GHOW) calls that were recorded at short distances, and then tested with high- and low-threat owl calls that were rebroadcast and re-recorded across six distances (25 m, 50 m, 75 m, 100 m, 150 m, and 200 m). Subjects were further tested with high-threat and low-threat synthetic tones produced to mimic the natural calls across the six distances. We predicted that birds would perceive and respond to: (1) high-threat predator calls at longer distances compared to low-threat predator calls, and (2) synthetic tones similarly compared to the stimuli that they were designed to mimic. We believed chickadees would continue to perceive and respond to predators that pose a high threat at further distances; however, only responding to low-threat stimuli was consistent across distance recordings. Synthetic tones were treated similarly to natural stimuli but at lower response levels. Thus, the results of this study provide insights into how chickadees perceive threat.

Acoustic discrimination of predators by black-capped chickadees (Poecile atricapillus).

Smaller owls and hawks are high-threat predators to small songbirds, like chickadees, in comparison to larger avian predators due to smaller raptors' agility (Templeton et al. in Proc Natl Acad Sci 104:5479-5482, 2005). The current literature focuses only on high- and low-threat predators. We propose that there may be a continuum in threat perception. In the current study, we conducted an operant go/no-go experiment investigating black-capped chickadees' acoustic discrimination of predator threat. After obtaining eight hawk and eight owl species' calls, we assigned each species as: (1) large, low-threat, (2) mid-sized, unknown-threat and (3) small-, high-threat predators, according to wingspan and body size. Black-capped chickadees were either trained to respond ('go') to high-threat predator calls or respond to low-threat predator calls. When either low-threat predator calls were not reinforced or high-threat predator calls were not reinforced the birds were to withhold responding ('no-go') to those stimuli. We then tested transfer of training with additional small and large predator calls, as well as with the calls of several mid-sized predators. We confirmed that chickadees can discriminate between high- and low-threat predator calls. We further investigated how chickadees categorize mid-sized species' calls by assessing transfer of training to previously non-differentially reinforced (i.e., pretraining) calls. Specifically, transfer test results suggest that mid-sized broad-winged hawks were perceived to be of high threat whereas mid-sized short-eared owls were perceived to be of low threat. However, mid-sized Cooper's hawks and northern hawk owls were not significantly differentially responded to, suggesting that they are of medium threat which supports the notion that perception of threat is along a continuum rather than distinct categories of high or low threat.

Pheromone cue triggers switch between vectors in the desert harvest ant, Veromessor pergandei.

The desert harvester ant (Veromessor pergandei) employs a mixture of social and individual navigational strategies at separate stages of their foraging trip. Individuals leave the nest along a pheromone-based column, travelling 3-40 m before spreading out to forage individually in a fan. Foragers use path integration while in this fan, accumulating a direction and distance estimate (vector) to return to the end of the column (column head), yet foragers' potential use of path integration in the pheromone-based column is less understood. Here we show foragers rely on path integration both in the foraging fan and while in the column to return to the nest, using separate vectors depending on their current foraging stage in the fan or column. Returning foragers displaced while in the fan oriented and travelled to the column head location while those displaced after reaching the column travel in the nest direction, signifying the maintenance of a two-vector system with separate fan and column vectors directing a forager to two separate spatial locations. Interestingly, the trail pheromone and not the surrounding terrestrial cues mediate use of these distinct vectors, as fan foragers briefly exposed to the pheromone cues of the column in isolation altered their paths to a combination of the fan and column vectors. The pheromone acts as a contextual cue triggering both the retrieval of the column-vector memory and its integration with the forager's current fan-vector.

Same but different: Socially foraging ants backtrack like individually foraging ants but use different mechanisms.

Diverse species may adopt behaviourally identical solutions to similar environmental challenges. However, the underlying mechanisms dictating these responses may be quite different and are often associated with the specific ecology or habitat of these species. Foraging desert ants use multiple strategies in order to successfully navigate. In individually foraging ants, these strategies are largely visually-based; this includes path integration and learned panorama cues, with systematic search and backtracking acting as backup mechanisms. Backtracking is believed to be controlled, at least in solitary foraging species, by three criteria: 1) foragers must have recent exposure to the nest panorama, 2) the path integrator must be near zero, and 3) the ant must be displaced to an unfamiliar location. Instead of searching for the nest, under these conditions, foragers head in the opposite compass direction of the one in which they were recently travelling. Here, we explore backtracking in the socially foraging desert harvester ant (Veromessor pergandei), which exhibits a foraging ecology consisting of a combination of social and individual cues in a column and fan structure. We find that backtracking in V. pergandei, similar to solitary foraging species, is dependent on celestial cues, and in particular on the sun's position. However, unlike solitary foraging species, backtracking in V. pergandei is not mediated by the same criteria. Instead the expression of this behaviour is dependent on the presence of the social cues of the column and the proportion of the column that foragers have completed prior to displacement.

Hear them roar: A comparison of black-capped chickadee (Poecile atricapillus) and human (Homo sapiens) perception of arousal in vocalizations across all classes of terrestrial vertebrates.

Recently, evidence for acoustic universals in vocal communication was found by demonstrating that humans can identify levels of arousal in vocalizations produced by species across three biological classes (Filippi et al., 2017). Here, we extend this work by testing whether two vocal learning species, humans and chickadees, can discriminate vocalizations of high and low arousal using operant discrimination go/no-go tasks. Stimuli included vocalizations from nine species: giant panda, American alligator, common raven, hourglass treefrog, African elephant, Barbary macaque, domestic pig, black-capped chickadee, and human. Subjects were trained to respond to high or low arousal vocalizations, then tested with additional high and low arousal vocalizations produced by each species. Chickadees (Experiment 1) and humans (Experiment 2) learned to discriminate between high and low arousal stimuli and significantly transferred the discrimination to additional panda, human, and chickadee vocalizations. Finally, we conducted discriminant function analyses using four acoustic measures, finding evidence suggesting that fundamental frequency played a role in responding during the task. However, these analyses also suggest roles for other acoustic factors as well as familiarity. In sum, the results from these studies provide evidence that chickadees and humans are capable of perceiving arousal in vocalizations produced by multiple species. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Sometimes a stick might just be a stick.

Suzuki (Proceedings of the Natural Academy of Sciences, 115, 1541-1545, 2018) conducted elegant field experiments examining referential communication in Japanese tits. Bond (Learning & Behavior, in press, 2019) explains some key considerations and future experimentation that should be conducted to solidify these conclusions. An important takeaway from both Suzuki and Bond is that scientists can, and should, both be excited for new, interesting scientific discoveries, and also view such findings with a critical, but collegial, eye for more parsimonious explanations and the manipulations required to test such explanations.

ZENK expression in the auditory pathway of black-capped chickadees (Poecile atricapillus) as a function of D note number and duty cycle of chick-a-dee calls.

Black-capped chickadees (Poecile atricapillus) use their namesake chick-a-dee call for multiple functions, altering the features of the call depending on context. For example, duty cycle (the proportion of time filled by vocalizations) and fine structure traits (e.g., number of D notes) can encode contextual factors, such as predator size and food quality. Wilson and Mennill (2011) found that chickadees show stronger behavioral responses to playback of chick-a-dee calls with higher duty cycles, but not to the number of D notes. That is, independent of the number of D notes in a call, but dependent on the overall proportion of time filled with vocalization, birds responded more to higher duty cycle playback compared to lower duty cycle playback. Here we presented chickadees with chick-a-dee calls that contained either two D (referred to hereafter as 2 D) notes with a low duty cycle, 2 D notes with a high duty cycle, 10 D notes with a high duty cycle, or 2 D notes with a high duty cycle but played in reverse (a non-signaling control). We then measured ZENK expression in the auditory nuclei where perceptual discrimination is thought to occur. Based on the behavioral results of Wilson and Mennill, 2011, we predicted we would observe the highest ZENK expression in response to forward-playing calls with high duty cycles; we predicted we would observe no significant difference in ZENK expression between forward-playing high duty cycle playbacks (2 D or 10 D). We found no significant difference between forward-playing 2 D and 10 D high duty cycle playbacks. However, contrary to our predictions, we did not find any effects of altering the duty cycle or note number presented.

Odometry and backtracking: social and individual navigation in group foraging desert harvester ants (Veromessor pergandei).

Veromessor pergandei harvester ants are group foragers which use a combination of social cues (pheromone-marked columns) and individual cues (e.g., self-generated movement, visual cues) when exploring foraging areas for resources. Upon finding food, individuals navigate back to the column, which guides their return to the nest. The direction and length of columns change between foraging bouts, and hence the end of the column (unlike the nest location) is non-stationary. We conducted displacement tests on returning foragers and present three novel findings. First, returning individual ants accurately estimate their distance from the foraging area to the end of the column. Second, ants that reached the column but only traveled a small proportion of the distance to the nest either show homeward or random orientation; random orientation was seen when the column was long. Third, ants that have traveled most of the way back to the nest along the column show backtracking when they are displaced-orienting in the direction opposite to the nest-similar to Australian desert ants Melophorus bagoti. This commonality suggests that some navigation strategies are general across species, and are utilized by ants that navigate individually or socially.

The effects of anthropogenic noise on feeding behaviour in black-capped chickadees (Poecile atricapillus).

Anthropogenic noise has been shown to impact animal behaviour. Most studies investigating anthropogenic noise, and the detrimental effect it has on behaviour, have been conducted in the field, where a myriad of covariates can make interpretation challenging. In this experiment, we studied the effects of an approximation of anthropogenic noise, simulated with brown noise, on the feeding behaviour of wild-caught black-capped chickadees in a laboratory setting. We measured the amount of time spent eating while subjects heard either conspecific calls, brown noise, or a combination of calls and brown noise. We found that subjects fed more in the silence following playback than during the playback itself for all types of stimuli, suggesting that chickadees may shift their feeding behaviour to avoid feeding during periods of noise. The ability to adapt to changing environments (e.g., varying noise levels) may allow species to thrive in the presence of anthropogenic noise. Our findings outline a laboratory-based method that could be adopted and adapted to examine a variety avian species and of types anthropogenic noise.

Humans recognize emotional arousal in vocalizations across all classes of terrestrial vertebrates: evidence for acoustic universals.

Writing over a century ago, Darwin hypothesized that vocal expression of emotion dates back to our earliest terrestrial ancestors. If this hypothesis is true, we should expect to find cross-species acoustic universals in emotional vocalizations. Studies suggest that acoustic attributes of aroused vocalizations are shared across many mammalian species, and that humans can use these attributes to infer emotional content. But do these acoustic attributes extend to non-mammalian vertebrates? In this study, we asked human participants to judge the emotional content of vocalizations of nine vertebrate species representing three different biological classes-Amphibia, Reptilia (non-aves and aves) and Mammalia. We found that humans are able to identify higher levels of arousal in vocalizations across all species. This result was consistent across different language groups (English, German and Mandarin native speakers), suggesting that this ability is biologically rooted in humans. Our findings indicate that humans use multiple acoustic parameters to infer relative arousal in vocalizations for each species, but mainly rely on fundamental frequency and spectral centre of gravity to identify higher arousal vocalizations across species. These results suggest that fundamental mechanisms of vocal emotional expression are shared among vertebrates and could represent a homologous signalling system.

ZENK expression following conspecific and heterospecific playback in the zebra finch auditory forebrain.

Zebra finches (Taeniopygia guttata) are sexually dimorphic songbirds, not only in appearance but also in vocal production: while males produce both calls and songs, females only produce calls. This dimorphism provides a means to contrast the auditory perception of vocalizations produced by songbird species of varying degrees of relatedness in a dimorphic species to that of a monomorphic species, species in which both males and females produce calls and songs (e.g., black-capped chickadees, Poecile atricapillus). In the current study, we examined neuronal expression after playback of acoustically similar hetero- and conspecific calls produced by species of differing phylogenetic relatedness to our subject species, zebra finch. We measured the immediate early gene (IEG) ZENK in two auditory areas of the forebrain (caudomedial mesopallium, CMM, and caudomedial nidopallium, NCM). We found no significant differences in ZENK expression in either male or female zebra finches regardless of playback condition. We also discuss comparisons between our results and the results of a previous study conducted by Avey et al. [1] on black-capped chickadees that used similar stimulus types. These results are consistent with the previous study which also found no significant differences in expression following playback of calls produced by various heterospecific species and conspecifics [1]. Our results suggest that, similar to black-capped chickadees, IEG expression in zebra finch CMM and NCM is tied to the acoustic similarity of vocalizations and not the phylogenetic relatedness of the species producing the vocalizations.

Chickadees discriminate contingency reversals presented consistently, but not frequently.

Chickadees are high-metabolism, non-migratory birds, and thus an especially interesting model for studying how animals follow patterns of food availability over time. Here, we studied whether black-capped chickadees (Poecile atricapillus) could learn to reverse their behavior and/or to anticipate changes in reinforcement when the reinforcer contingencies for each stimulus were not stably fixed in time. In Experiment 1, we examined the responses of chickadees on an auditory go/no-go task, with constant reversals in reinforcement contingencies every 120 trials across daily testing intervals. Chickadees did not produce above-chance discrimination; however, when trained with a procedure that only reversed after successful discrimination, chickadees were able to discriminate and reverse their behavior successfully. In Experiment 2, we examined the responses of chickadees when reversals were structured to occur at the same time once per day, and chickadees were again able to discriminate and reverse their behavior over time, though they showed no reliable evidence of reversal anticipation. The frequency of reversals throughout the day thus appears to be an important determinant for these animals' performance in reversal procedures.

Discrimination of acoustically similar conspecific and heterospecific vocalizations by black-capped chickadees (Poecile atricapillus).

Chickadees produce a multi-note chick-a-dee call in multiple socially relevant contexts. One component of this call is the D note, which is a low-frequency and acoustically complex note with a harmonic-like structure. In the current study, we tested black-capped chickadees on a between-category operant discrimination task using vocalizations with acoustic structures similar to black-capped chickadee D notes, but produced by various songbird species, in order to examine the role that phylogenetic distance plays in acoustic perception of vocal signals. We assessed the extent to which discrimination performance was influenced by the phylogenetic relatedness among the species producing the vocalizations and by the phylogenetic relatedness between the subjects' species (black-capped chickadees) and the vocalizers' species. We also conducted a bioacoustic analysis and discriminant function analysis in order to examine the acoustic similarities among the discrimination stimuli. A previous study has shown that neural activation in black-capped chickadee auditory and perceptual brain regions is similar following the presentation of these vocalization categories. However, we found that chickadees had difficulty discriminating between forward and reversed black-capped chickadee D notes, a result that directly corresponded to the bioacoustic analysis indicating that these stimulus categories were acoustically similar. In addition, our results suggest that the discrimination between vocalizations produced by two parid species (chestnut-backed chickadees and tufted titmice) is perceptually difficult for black-capped chickadees, a finding that is likely in part because these vocalizations contain acoustic similarities. Overall, our results provide evidence that black-capped chickadees' perceptual abilities are influenced by both phylogenetic relatedness and acoustic structure.

An investigation of sex differences in acoustic features in black-capped chickadee (Poecile atricapillus) chick-a-dee calls.

Sex differences have been identified in a number of black-capped chickadee vocalizations and in the chick-a-dee calls of other chickadee species [i.e., Carolina chickadees (Poecile carolinensis)]. In the current study, 12 acoustic features in black-capped chickadee chick-a-dee calls were investigated, including both frequency and duration measurements. Using permuted discriminant function analyses, these features were examined to determine if any features could be used to identify the sex of the caller. Only one note type (A notes) classified male and female calls at levels approaching significance. In particular, a permuted discriminant function analysis revealed that the start frequency of A notes best allowed for categorization between the sexes compared to any other acoustic parameter. This finding is consistent with previous research on Carolina chickadee chick-a-dee calls that found that the starting frequency differed between male- and female-produced A notes [Freeberg, Lucas, and Clucas (2003). J. Acoust. Soc. Am. 113, 2127-2136]. Taken together, these results and the results of studies with other chickadee species suggest that sex differences likely exist in the chick-a-dee call, specifically acoustic features in A notes, but that more complex features than those addressed here may be associated with the sex of the caller.