Alarm calls of a cooperative bird are referential and elicit context-specific antipredator behavior
Although functionally referential signals have been extensively studied, largely in mammals (e.g., nonhuman primates, see Cheney and Seyfarth (1988); mongooses, see Manser et al. (2002); and other ground-dwelling species, see Blumstein and Armitage (1997), other social taxa such as birds would similarly benefit from the use of referential signals. We therefore investigated alarm calling in the cooperative noisy miner (Manorina melanocephala), a species that has been anecdotally recorded producing aerial alarms to flying predators and empirically recorded generating terrestrial alarms to ground-based threats. For these signals to be truly referential however, they must meet 3 criteria. First, calls must be structurally distinct, a requirement that these 2 call types meet. Second, calls must be stimulus-specific and reliably associated with a given stimulus. We tested this on free-living birds by exposing them to a simulated aerial predator that was either in flight or subsequently perched and thus presented one of the first studies on functionally referential alarm systems where both aerial and terrestrial alarm calls have been tested. Miners only produced aerial alarms while the stimulus was in flight, switching to terrestrial alarms once it landed. Third, referential signals must elicit different escape responses that are "appropriate" to the associated threat. Under field conditions, aerial alarm playback alone provoked an almost instantaneous response of fleeing to vegetation cover, whereas terrestrial alarm playback elicited significantly slower responses by receivers and an increase in scanning behavior. During laboratory experiments, aerial alarms stimulated birds to spend more time looking upwards, whereas terrestrial alarm calls stimulated individuals to scan perpendicularly, as expected if these stimuli provided information on likely predator location. Although other avian taxa have been shown to use referential alarm signals, this system provides novel evidence of referential calls based on the behavior rather than the type of predator, providing a highly adaptive means of communicating risk to other members of the social group in this cooperative species.
Exploring the Brain and Behaviour of a Reverse Keystone Species, The Noisy Miner (Manorina Melanocephala)
The aim of this thesis was to study the cognitive complexity of the noisy miner (Manorina melanocephala) in an attempt to better understand its success in urban environments. Furthermore, the thesis aimed to use this species, not widely known for its cognitive prowess despite possessing complex behaviours and the proposed tool-kit for intelligence, to better understand potential indicators of cognition, namely, whether brain size is an accurate gauge of intelligence.
We first sought to conduct species-specific behavioural studies to test aspects of noisy miner behaviour that may assist their navigation of novel environments. Adapting the mirrormark test, we identified that noisy miners quickly habituate to reflective surfaces, following a behavioural sequence that initially begins with conspecific/social behaviours, and ends with the bird disengaging, and thus saving energetic costs, from the surface. We then investigated whether noisy miners were capable of “true” individual recognition, a complex behaviour that involves the ability of receivers to not only recognise a signaller, yet place a reliability status to this signaller regardless of context. Noisy miners not only reduced responses to unreliable signallers, they maintained this response across vocal contexts, indicating that they are capable of distinguishing individuals based on vocalisations alone, a characteristic likely maintained through their use of vocalisations to facilitate cooperative events such as group mobbing of predators.
Finally, we challenged the cognitive capacity of noisy miners through studying whether they could identify individuals of another species, humans, and allocate these novel people as “good” (providing food) or “bad” (captured individuals in nets) based on interactions. We identified that noisy miners rapidly learned to summon colony members upon seeing the “good” mask, yet would respond harshly with terrestrial alarm calls (more syllables at higher frequencies and rates) upon seeing the “bad” mask after the aversive events.
We next developed a high-throughput, non-biased quantification method to measure neuronal density and identify nuclear sizes using flow cytometry. The results obtained were comparable to those identified using stereological counting methods and consequently we employed this method to determine neuronal density of the noisy miner. Despite being an avian species, the procedure proved efficient across taxa and provided clear and repeatable evidence that noisy miners possess greater neuronal densities than Wistar rats (Rattus norvegicus), a species known for their success in cognitive challenges such as the radial eight-arm maze, where the species flexibly adapts to changes in food location. However, the noisy miner, a species to which this challenge is not standard, proved to make fewer errors during trials, thus demonstrating greater behavioural flexibility. We interpret the greater behavioural flexibility of the noisy miner compared to the Wistar rat as a result of the species possessing greater neuronal densities, with size of cells across the two species not being significantly different, therefore resulting in noisy miners having a shorter distance between cells for signal transmission.
The density of neurons, composed of cells packed closely together, likely facilitates the cognitive complexity and behavioural flexibility that this thesis confirmed through the behavioural studies on the noisy miner. Subsequently, this ability to rapidly adapt allows for the success of the noisy miner even in the most rapidly growing urban areas. We propose that in having a comparable measure of cognitive complexity (i.e. method to measure neuronal density across taxa), that this approach could be applied to other species so that we can gain an understanding of those species most likely to be affected by further urbanisation and anthropogenic changes.
Quantitative determination of neuronal size and density using flow cytometry
Background: Recent anthropomorphic disturbances are occurring at an increasing rate leading to organisms facing a variety of challenges. This change is testing the information processing capacity (IPC) of all animals. Brain function is widely accepted to be influenced by a variety of factors, including relative size, number of neurons and neuronal densities. Therefore, in order to understand what drives an animals IPC, a methodological approach to analyze these factors must be established.
New method: Here we created a protocol that allowed for high-throughput, non-biased quantification of neuronal density and size across six regions of the brain. We used the Isotropic Fractionator method in combination with flow cytometry to identify neuronal and non-neuronal cells in the brains of adult rats.
Comparison with existing methods: The results obtained were comparable to those identified using stereological counting methods.
Results: By employing this new method, the number of nuclei in a specific brain region can be compared between replicate animals within an experiment. By calibrating the forward scatter channel of the flow cytometer with size standard beads, neuronal and non-neuronal nuclear sizes can be estimated simultaneously with nuclei enumeration. These techniques for nuclear counting and size estimation are technically and biologically reproducible.
Conclusion: Use of flow cytometry provides a methodological approach that allows for consistency in research, so that information on brain morphology, and subsequent function, will become comparable across taxa.
Cooperative bird discriminates between individuals based purely on their aerial alarm calls
From an evolutionary perspective, the ability to recognize individuals provides great selective advantages, such as avoiding inbreeding depression during breeding. Whilst the capacity to recognize individuals for these types of benefits is well established in social contexts, why this recognition might arise in a potentially deadly alarm-calling context following predator encounters is less obvious. For example, in most avian systems, alarm signals directed toward aerial predators represent higher predation risk and vulnerability than when individuals vocalize toward a terrestrial-based predator. Although selection should favor simple, more effective alarm calls to these dangerous aerial predators, the potential of these signals to nonetheless encode additional information such as caller identity has not received a great deal of attention. We tested for individual discrimination capacity in the aerial alarm vocalizations of the noisy miner (Manorina melanocephala), a highly social honeyeater that has been previously shown to be able to discriminate between the terrestrial alarm signals of individuals. Utilizing habituation-discrimination paradigm testing, we found conclusive evidence of individual discrimination in the aerial alarm calls of noisy miners, which was surprisingly of similar efficiency to their ability to discriminate between less urgent terrestrial alarm signals. Although the mechanism(s) driving this behavior is currently unclear, it most likely occurs as a result of selection favoring individualism among other social calls in the repertoire of this cooperative species. This raises the intriguing possibility that individualistic signatures in vocalizations of social animals might be more widespread than currently appreciated, opening new areas of bioacoustics research.