Measuring Behaviour: An Introductory Guide, Paul Martin, Patrick Bateson. University of Cambridge Press, Cambridge (1986), x, +200. Price £20.00 (hardback), £6.95 (paperback)

In many species, individuals gather information about their environment both through direct experience and through information obtained from others. Social learning, or the acquisition of information from others, can occur both within and between species and may facilitate the rapid spread of antipredator behaviour. Within birds, acoustic signals are frequently used to alert others to the presence of predators, and individuals can quickly learn to associate novel acoustic cues with predation risk. However, few studies have addressed whether such learning occurs only though direct experience or whether it has a social component, nor whether such learning can occur between species. We investigate these questions in two sympatric species of Parids: blue tits (Cyanistes caeruleus) and great tits (Parus major). Using playbacks of unfamiliar bird vocalizations paired with a predator model in a controlled aviary setting, we find that blue tits can learn to associate a novel sound with predation risk via direct experience, and that antipredator response to the sound can be socially transmitted to heterospecific observers, despite lack of first-hand experience. Our results suggest that social learning of acoustic cues can occur between species. Such interspecific social information transmission may help to mediate the formation of mixed-species aggregations.

https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2019.2513

Social learning of acoustic anti-predator cues occurs between wild bird species

Animal alarm calls can contain detailed information about a predator's threat, and heterospecific eavesdropping on these signals creates vast communication networks. While eavesdropping is common, this indirect public information is often less reliable than direct predator observations. Red-breasted nuthatches (Sitta canadensis) eavesdrop on chickadee mobbing calls and vary their behaviour depending on the threat encoded in those calls. Whether nuthatches propagate this indirect information in their own calls remains unknown. Here we test whether nuthatches propagate direct (high and low threat raptor vocalizations) or indirect (high and low threat chickadee mobbing calls) information about predators differently. When receiving direct information, nuthatches vary their mobbing calls to reflect the predator's threat. However, when nuthatches obtain indirect information, they produce calls with intermediate acoustic features, suggesting a more generic alarm signal. This suggests nuthatches are sensitive to the source and reliability of information and selectively propagate information in their own mobbing calls.

/pdf/nuthatches-vary-their-alarm-calls-based-upon-the-source-of-2i0ue7pm51.pdf

Nuthatches vary their alarm calls based upon the source of the eavesdropped signals

When they detect a predator, many species emit anti-predator vocalizations. In some cases, they emit mobbing calls, which are associated with the caller approaching and harassing the predator while attracting others to join it. Surprisingly, although mobbing has been widely reported in adults of numerous species, there has been no test of the role of learning in mobbing call recognition, especially during ontogeny. Here, we exposed wild great tit (Parus major) nestlings to playbacks of an unthreatening novel sound either associated with conspecific mobbing calls (experimental treatment) or with another unthreatening novel sound (control treatment). We then tested them as nestlings and fledglings to see how they respond to the novel sound compared to conspecific mobbing calls. Results revealed that fledglings in the experimental treatment behaved similarly to conspecific mobbing calls and the novel sound associated with conspecific mobbing calls. Because mobbing efficiency is often linked to interspecific communication, associative learning should be used by heterospecifics as mobbing calls recognition mechanism. Regardless of treatment during the nestling phase, fledglings always were sensitive to the playback of conspecific mobbing calls. However, fledglings from the control group were more likely to approach the loudspeaker than those from the experimental group when mobbing calls were played suggesting that overexposure during the nestling phase altered mobbing learning. Overall, these results suggest that learning could play a role in the recognition of calls, like heterospecific mobbing calls, when paired with conspecific mobbing, and that mobbing is perceived as a threatening stimulus from a very young age.

The role of associative learning process on the response of fledgling great tits (Parus major) to mobbing calls.

From ants to zebras, animals are influenced by the behavior of others. At the simplest level, social support can reduce neophobia, increasing animals’ exploration of novel spaces, foods, and other environmental stimuli. Animals can also learn new skills more quickly and more readily after observing others perform them. How then can we apply animals’ proclivity to socially learn to enhance their care and welfare in captive settings? Here, I review the ways in which animals (selectively) use social information, and propose tactics for leveraging that to refine the behavioral management of captive animals: to enhance socialization techniques, enrichment strategies, and training outcomes. It is also important to consider, however, that social learning does not always promote the uniform expression of new behaviors. There are differences in animals’ likelihood to seek out or use socially provided information, driven by characteristics such as species, rank, age, and personality. Additionally, social learning can result in inexact transmission or the transmission of undesirable behaviors. Thus, understanding when, how, and why animals use social information is key to developing effective strategies to improve how we care for animals across settings and, ultimately, enhance captive animal welfare.

Leveraging Social Learning to Enhance Captive Animal Care and Welfare

Feeling anxious? The mechanisms of vocal deception in tufted capuchin monkeys.

Many vertebrate taxa respond to heterospecific alarm calls with anti-predator behaviours. While it is unclear how apparent recognition is achieved, learned associations between the occurrence of the call and the presence of a predator are considered the most likely explanation. Conclusive evidence that this behaviour is indeed underpinned by learning, however, is scarce. This study tested whether wild black capuchin monkeys (Sapajus nigritus) learn to associate novel sounds with predators through a two-phase field experiment. During an initial training phase, three study groups were each presented with a playback of one of the three novel sounds together with a simulated felid predator on four occasions over an 8- to 12-week period. This was followed by a test phase, wherein each of the three sounds was played back to individuals in all three groups, allowing each sound to serve as both a test stimulus for individuals trained with that sound, and a control stimulus for individuals trained with another sound. Antipredator responses were significantly stronger in response to test sounds than to controls. Limited observations suggest that antipredator responses persisted for at least 2 years without reinforcement of the predator–sound link. Additionally, responses to noisier sounds were typically stronger than were those to more tonal sounds, although the effect of sound type cannot be disentangled from potential effects of group. This study provides the strongest evidence to date that learning affects the responses of primates to sounds such as heterospecific alarm calls, and supports the contention that signals provide receivers with information.

/pdf/experimental-evidence-for-heterospecific-alarm-signal-4cckyi9f7s.pdf

Experimental evidence for heterospecific alarm signal recognition via associative learning in wild capuchin monkeys

Ecological models of mating systems provide a theoretical framework to predict the effect of the defendability of both breeding resources and mating partners on mating patterns. In resource-based mating systems, male control over breeding resources is tightly linked to female mating preference. To date, few field studies have experimentally investigated the relationship between male resource control and female mating preference in mammals due to difficulties in manipulating ecological factors (e.g., food contestability). We tested the within-group male resource defense hypothesis experimentally in a wild population of black capuchin monkeys (Sapajus nigritus) in Iguazu National Park, Argentina. Sapajus spp. represent an ideal study model as, in contrast to most primates, they have been previously argued to be characterized by female mate choice and a resource-based mating system in which within-group resource monopolization by high-ranking males drives female mating preference for those males. Here, we examined whether females (N = 12) showed a weaker preference for alpha males during mating seasons in which food distribution was experimentally manipulated to be less defendable relative to those in which it was highly defendable. Results did not support the within-group male resource defense hypothesis, as female sexual preferences for alpha males did not vary based on food defendability. We discuss possible reasons for our results, including the possibility of other direct and indirect benefits females receive in exercising mate choice, the potential lack of tolerance over food directed towards females by alpha males, and phylogenetic constraints.

/pdf/male-resource-defense-mating-system-in-primates-an-e8miuvspzf.pdf

Martin Fahy

Papers

Feeling anxious? The mechanisms of vocal deception in tufted capuchin monkeys.

Experimental evidence for heterospecific alarm signal recognition via associative learning in wild capuchin monkeys

Male resource defense mating system in primates? An experimental test in wild capuchin monkeys.