Michele K. Moscicki

Dominance signalled in an acoustic ornament

In many species, males use auditory signals to attract females and females select males based on their dominance status. Here we show that information on dominance status in male black-capped chickadees, Poecile atricapillus, a small, temperate, North American songbird, can be extracted from individual songs. We found that the relative amplitude of the two notes in the ‘fee bee’ song of this species was more consistent in dominant males. Furthermore, females responded differently to presentations of single song exemplars from males of different dominance status, with females vocalizing more and performing more motor behaviours during the presentation of dominant songs. Our study suggests that non-pitch-based cues within single vocalizations can both reliably indicate relative rank and be discriminated by females. 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. The concept of dominance was first developed by SchjelderupEbbe (1935) when studying fowl (Gallus gallus), who coined the term ‘pecking order’. Today, dominance has taken on broader meanings. Dominance is a relative measure based on encounters between individuals in which one individual asserts itself over another. Such hierarchies among individuals that repeatedly interact with one another serve to reduce future aggressive interactions. How individual animals display their dominance status to conspecifics is a matter of great importance for intra- and intersexual communication. In particular, being a dominant male

Neural Correlates of Threat Perception: Neural Equivalence of Conspecific and Heterospecific Mobbing Calls Is Learned

Songbird auditory areas (i.e., CMM and NCM) are preferentially activated to playback of conspecific vocalizations relative to heterospecific and arbitrary noise [1]–[2]. Here, we asked if the neural response to auditory stimulation is not simply preferential for conspecific vocalizations but also for the information conveyed by the vocalization. Black-capped chickadees use their chick-a-dee mobbing call to recruit conspecifics and other avian species to mob perched predators [3]. Mobbing calls produced in response to smaller, higher-threat predators contain more “D” notes compared to those produced in response to larger, lower-threat predators and thus convey the degree of threat of predators [4]. We specifically asked whether the neural response varies with the degree of threat conveyed by the mobbing calls of chickadees and whether the neural response is the same for actual predator calls that correspond to the degree of threat of the chickadee mobbing calls. Our results demonstrate that, as degree of threat increases in conspecific chickadee mobbing calls, there is a corresponding increase in immediate early gene (IEG) expression in telencephalic auditory areas. We also demonstrate that as the degree of threat increases for the heterospecific predator, there is a corresponding increase in IEG expression in the auditory areas. Furthermore, there was no significant difference in the amount IEG expression between conspecific mobbing calls or heterospecific predator calls that were the same degree of threat. In a second experiment, using hand-reared chickadees without predator experience, we found more IEG expression in response to mobbing calls than corresponding predator calls, indicating that degree of threat is learned. Our results demonstrate that degree of threat corresponds to neural activity in the auditory areas and that threat can be conveyed by different species signals and that these signals must be learned.

Sex, boldness and stress experience affect convict cichlid, Amatitlania nigrofasciata, open field behaviour

How an organism deals with stressors is an integral component of survival. Recent research has shown that differences in a well-studied personality axis in fish, the shy–bold axis, relate to stress-coping behaviours. Bold fish tend to cope in a proactive manner (e.g. fighting) while shy fish cope more reactively (e.g. freezing). Because bold fish behave in a more risk-prone manner, it is likely that they encounter more stressors on average than shy fish. Greater exposure to stressful conditions may result in bold fish being less behaviourally sensitive to stressors (i.e. stress resilience). To investigate the idea of stress exposure leading to resilience, we examined whether fish personality (i.e. more bold or shy) affected anxiety-related behaviour in an open field task after fish had been exposed to a net-chasing stressor. We investigated open field behaviour in the presence and absence of a stressor (i.e. damage-induced alarm cues) to determine whether bolder fish would cope differently with a stressor than shy fish after recent stress exposure of a different type. Furthermore, we examined whether asymmetry in the habenula, an asymmetrical nucleus related to behavioural responses to stress and anxiety, is related to behaviour in the presence of stressors. We found no relationship between habenular asymmetry and behaviour in the open field. Net chasing increased activity in the open field for both sexes. We found an interaction between stress exposure and freezing behaviour in females but not in males. When females were not net-chased, shyer females showed a decrease in freezing behaviour when exposed to alarm cues, whereas bolder females showed no change in behaviour. When females were net-chased, there was no difference in freezing behaviour between bolder and shyer fish. We suggest that different parental care roles in this species lead to differential perceptions of the threat of stress between the sexes.

ZENK Activation in the Nidopallium of Black-Capped Chickadees in Response to Both Conspecific and Heterospecific Calls

Neuronal populations in the songbird nidopallium increase in activity the most to conspecific vocalizations relative to heterospecific songbird vocalizations or artificial stimuli such as tones. Here, we tested whether the difference in neural activity between conspecific and heterospecific vocalizations is due to acoustic differences or to the degree of phylogenetic relatedness of the species producing the vocalizations. To compare differences in neural responses of black-capped chickadees, Poecile atricapillus, to playback conditions we used a known marker for neural activity, ZENK, in the caudal medial nidopallium and caudomedial mesopallium. We used the acoustically complex ‘dee’ notes from chick-a-dee calls, and vocalizations from other heterospecific species similar in duration and spectral features. We tested the vocalizations from three heterospecific species (chestnut-backed chickadees, tufted titmice, and zebra finches), the vocalizations from conspecific individuals (black-capped chickadees), and reversed versions of the latter. There were no significant differences in the amount of expression between any of the groups except in the control condition, which resulted in significantly less neuronal activation. Our results suggest that, in certain cases, neuronal activity is not higher in response to conspecific than in response to heterospecific vocalizations for songbirds, but rather is sensitive to the acoustic features of the signal. Both acoustic features of the calls and the phylogenetic relationship between of the signaler and the receiver interact in the response of the nidopallium.

Lateralized behaviour of a non-social cichlid fish (Amatitlania nigrofasciata) in a social and a non-social environment

Cerebral lateralization, the partitioning of cognitive function preferentially into one hemisphere of the brain, is a trait ubiquitous among vertebrates. Some species exhibit population level lateralization, where the pattern of cerebral lateralization is the same for most members of that species; however, other species show only individual level lateralization, where each member of the species has a unique pattern of lateralized brain function. The pattern of cerebral lateralization within a population and an individual has been shown to differ based on the stimulus being processed. It has been hypothesized that sociality within a species, such as shoaling behaviour in fish, may have led to the development and persistence of population level lateralization. Here we assessed cerebral lateralization in convict cichlids (Amatitlania nigrofasciata), a species that does not shoal as adults but that shoals briefly as juveniles. We show that both male and female convict cichlids display population level lateralization when in a solitary environment but only females show population level lateralization when in a perceived social environment. We also show that the pattern of lateralization differs between these two tasks and that strength of lateralization in one task is not predictive of strength of lateralization in the other task.

Seeing orange: breeding convict cichlids exhibit heightened aggression against more colorful intruders

Female convict cichlids (Amatitlania siquia) exhibit bright orange ventral coloration that males lack. The behavioral implications of this color are poorly understood, particularly in naturally occurring populations where female coloration could play a role in the expression of territorial nest-guarding behaviors. In this field experiment, monogamous breeding pairs of convict cichlids were presented with 3D printed model conspecific intruders of three body sizes (small, medium, and large) exhibiting three orange patch sizes (large, small, or none) to observe how territorial aggression varied as a function of intruder size and female coloration. Individuals occupying breeding pairs that were defending hatched offspring were significantly more aggressive toward intruders with small and large amounts of orange than toward models lacking orange, indicating that color is an important context-dependent elicitor of aggression in this species. Males were significantly more aggressive toward the intruder than females, and male aggression was strongly influenced by their size relative to the intruder. When males were smaller than the intruder, they performed significantly more aggressive acts than when they were the same size or larger than the intruder; this trend persisted across three putative populations in Lake Xiloa, Nicaragua. A potential explanation for these findings is that the orange color functions as a signal of individual quality or breeding readiness and that breeding pairs increase aggression to repel intruders that pose the greatest threat to pair bond and nest maintenance.Significance statementOne or both sexes of many animal species possess brightly colored features that might communicate information about overall heath or reproductive status. In convict cichlid fish, males and females establish pair bonds and jointly defend their nest and offspring. Single females exhibit striking orange coloration that males and breeding females lack. Our field-based experiment provided evidence that more colorful females, which likely pose a threat to pair bond stability and nest maintenance, incite more aggression from breeding pairs than drab females. Our study suggests that color provides salient information about, perhaps, female quality or readiness to breed in natural populations, and adds to a growing body of research that seeks to understand the varied roles that colorful ornaments play in animal communication.

Note types and coding in Parid vocalizations: the chick-a-dee call of the boreal chickadee (Poecile hudsonicus).

An important first step in characterizing a vocalization is to classify, describe, and measure the elements of that vocalization. Here, this methodology is employed to study the chick-a-dee call of the boreal chickadee (Poecile hudsonicus). The note types (A, B, C, D, and D(h)) in a sample of boreal chickadee calls are identified and described, spectral and temporal features of each note type are analyzed, and production phenomena in each note type are identified and quantified. Acoustic variability is compared across note types and individuals to determine potential features used for note-type and individual discrimination. Frequency measures appear to be the most useful features for identifying note types and individuals, though total duration may also be useful. Call syntax reveals that boreal chick-a-dee calls follow a general rule of note-type order, namely A-B-C-D(h)-D, and that any note type in this sequence may be repeated or omitted. This work provides a thorough description of the boreal chickadee chick-a-dee call and will serve as a foundation for future studies aimed at elucidating this calls functional significance within this species, as well as for studies comparing chick-a-dee calls across Poecile species.

Note Types and Coding in Parid Vocalizations: The chick-a-dee Call of the Mexican Chickadee Poecile sclateri

Abstract. To understand the communicative functions of any vocalization it is important to describe and classify the elements of that vocalization. Mexican Chickadees produce a namesake chick-a-dee call. Here, the note types (A, C, D, and Dh) from a sample of Mexican Chickadee chick-a-dee calls are identified, described, and classified. Frequency and temporal features of each note type are measured and compared to determine which features may be useful for note-type discrimination. Frequency measures, particularly peak frequency, appear to be most useful for discriminating among note types. Call syntax is analyzed to determine rules for note-type production. Mexican Chickadees produce the notes within their chick-a-dee calls in a consistent order: A → C → Dh → D with the potential for any note type to be repeated or omitted within this sequence. Similar to species in the brown-headed chickadee clade, B notes were not found in the calls of Mexican chickadees, suggesting this species may belong to the brown-headed clade. This work describes the chick-a-dee call of Mexican Chickadees and provides a foundation for future work aimed at understanding the communicative significance of this call within this species, as well as for comparative work on the chick-a-dee call among chickadee species.

Damage-induced alarm cues influence lateralized behaviour but not the relationship between behavioural and habenular asymmetry in convict cichlids (Amatitlania nigrofasciata)

Cerebral lateralization, the partitioning of functions into a certain hemisphere of the brain, is ubiquitous among vertebrates. Evidence suggests that the cognitive processing of a stimulus is performed with a specific hemisphere depending in part upon the emotional valence of the stimulus (i.e. whether it is appetitive or aversive). Recent work has implicated a predominance of right-hemisphere processing for aversive stimuli. In fish with laterally placed eyes, the preference to view an object with a specific eye has been used as a proxy for assessing cerebral lateralization. The habenula, one of the most well-known examples of an asymmetrical neural structure, has been linked to behavioural asymmetry in some fish species. Here, we exposed convict cichlid fish (Amatitlania nigrofasciata) to both a social and non-social lateralization task and assessed behavioural lateralization in either the presence or absence of an aversive stimulus, damage-induced alarm cues. We also assessed whether behavioural asymmetry in these tests was related to asymmetry of the habenular nuclei. We found that when alarm cues were present, fish showed increased left-eye (and by proxy, right hemisphere) preference for stimulus viewing. In addition, females, but not males, showed stronger eye preferences when alarm cues were present. We did not find a relationship between behavioural lateralization and habenular lateralization. Our results conflict with previous reports of concordance between behavioural and habenular lateralization in this fish species. However, our results do provide support for the hypothesis of increased right-hemisphere use when an organism is exposed to aversive stimuli.