Giant hornet ( Vespa soror ) attacks trigger frenetic antipredator signalling in honeybee ( Apis cerana ) colonies

Asian honeybees use an impressive array of strategies to protect nests from hornet attacks, although little is understood about how antipredator signals coordinate defences. We compared vibroacoustic signalling and defensive responses of Apis cerana colonies that were attacked by either the group-hunting giant hornet Vespa soror or the smaller, solitary-hunting hornet Vespa velutina . Apis cerana colonies produced hisses, brief stop signals and longer pipes under hornet-free conditions. However, hornet-attack stimuli—and V. soror workers in particular—triggered dramatic increases in signalling rates within colonies. Soundscapes were cacophonous when V. soror predators were directly outside of nests, in part because of frenetic production of antipredator pipes, a previously undescribed signal. Antipredator pipes share acoustic traits with alarm shrieks, fear screams and panic calls of primates, birds and meerkats. Workers making antipredator pipes exposed their Nasonov gland, suggesting the potential for multimodal alarm signalling that warns nestmates about the presence of dangerous hornets and assembles workers for defence. Concurrent observations of nest entrances showed an increase in worker activities that support effective defences against giant hornets. Apis cerana workers flexibly employ a diverse alarm repertoire in response to attack attributes, mirroring features of sophisticated alarm calling in socially complex vertebrates.

The cessation of contact calls does not provoke or modulate alarm behaviour in a social passerine

Vocalizations that signal predation risk such as alarm calls provide crucial information for the survival of group-living individuals. However, alarm calling may attract the predator’s attention and, to avoid this cost, animals can opt for alternative strategies to indicate danger, such as ‘adaptive silence’, which is the cessation of vocalizations. We investigate here whether abrupt contact call cessation would provoke alarm responses, or would reinforce the signal given by an alarm call. In an aviary setting, we conducted playback experiments with a group-living passerine, the Swinhoe’s white-eye, Zosterops simplex. We found that birds did not respond to a sudden call cessation, nor did they have a stronger response to alarm calls followed by silence than to alarm calls followed by contact calls. Confirming previous work investigating contact call rate, it appears that in this species contact calls encode information about social factors but not environmental conditions.

The many functions of vocal learning

The capacity to learn novel vocalizations has evolved convergently in a wide range of species. Courtship songs of male birds or whales are often treated as prototypical examples, implying a sexually selected context for the evolution of this ability. However, functions of learned vocalizations in different species are far more diverse than courtship, spanning a range of socio-positive contexts from individual identification, social cohesion, or advertising pair bonds, as well as agonistic contexts such as territorial defence, deceptive alarm calling or luring prey. Here, we survey the diverse usages and proposed functions of learned novel signals, to build a framework for considering the evolution of vocal learning capacities that extends beyond sexual selection. For each function that can be identified for learned signals, we provide examples of species using unlearned signals to accomplish the same goals. We use such comparisons to generate hypotheses concerning when vocal learning is adaptive, given a particular suite of socio-ecological traits. Finally, we identify areas of uncertainty where improved understanding would allow us to better test these hypotheses. Considering the broad range of potential functions of vocal learning will yield a richer appreciation of its evolution than a narrow focus on a few prototypical species. This article is part of the theme issue ‘Vocal learning in animals and humans’.

Referential alarm calling elicits future vigilance in a host of an avian brood parasite

Yellow warblers ( Setophaga petechia ) use referential ‘seet’ calls to warn mates of brood parasitic brown-headed cowbirds ( Molothrus ater ). In response to seet calls during the day, female warblers swiftly move to sit tightly on their nests, which may prevent parasitism by physically blocking female cowbirds from inspecting and laying in the nest. However, cowbirds lay their eggs just prior to sunrise, not during daytime. We experimentally tested whether female warblers, warned by seet calls on one day, extend their anti-parasitic responses into the future by engaging in vigilance at sunrise on the next day, when parasitism may occur. As predicted, daytime seet call playbacks caused female warblers to leave their nests less often on the following morning, relative to playbacks of both their generic anti-predator calls and silent controls. Thus, referential calls do not only convey the identity or the type of threat at present but also elicit vigilance in the future to provide protection from threats during periods of heightened vulnerability.

Lesser spot-nosed monkeys coordinate alarm call production with associated Campbell’s monkeys

Forest monkeys often form semi-permanent mixed-species associations to increase group-size related anti-predator benefits without corresponding increases in resource competition. In this study, we analysed the alarm call system of lesser spot-nosed monkeys, a primate that spends most of its time in mixed-species groups while occupying the lowest and presumably most dangerous part of the forest canopy. In contrast to other primate species, we found no evidence for predator-specific alarm calls. Instead, males gave one general alarm call type (‘kroo’) to three main dangers (i.e., crowned eagles, leopards and falling trees) and a second call type (‘tcha-kow’) as a coordinated response to calls produced in non-predatory contexts (‘boom’) by associated male Campbell’s monkeys. Production of ‘kroo’ calls was also strongly affected by the alarm calling behaviour of male Campbell’s monkeys, suggesting that male lesser spot-nosed monkeys adjust their alarm call production to another species’ vocal behaviour. We discuss different hypotheses for this unusual phenomenon and propose that high predation pressure can lead to reliance on other species vocal behaviour to minimise predation. Significance statement Predation can lead to the evolution of acoustically distinct, predator-specific alarm calls. However, there are occasional reports of species lacking such abilities, despite diverse predation pressure, suggesting that evolutionary mechanisms are more complex. We conducted field experiments to systematically describe the alarm calling behaviour of lesser spot-nosed monkeys, an arboreal primate living in the lower forest strata where pressure from different predators is high. We found evidence for two acoustically distinct calls but, contrary to other primates in the same habitat, no evidence for predator-specific alarms. Instead, callers produced one alarm call type (‘kroo’) to all predator classes and another call type (‘tcha-kow’) to non-predatory dangers, but only as a response to a specific vocalisation of Campbell’s monkeys (‘boom’). The production of both calls was affected by the calling behaviour of Campbell’s monkeys, suggesting that lesser spot-nosed monkey vocal behaviour is dependent on the antipredator behaviour of other species. Our study advances the theory of interspecies interactions and evolution of alarm calls.

Female putty-nosed monkeys ( Cercopithecus nictitans ) vocally recruit males for predator defence

Alarm calls can trigger very different behavioural changes in receivers and signallers might apply different alarm call strategies based on their individual cost-benefit ratio. These cost-benefit ratios can also vary as a function of sex. For instance, male but not female forest guenons possess loud alarms that serve warning and predator deterrence functions, but also intergroup spacing and male–male competition. In some forest guenons, the context specificity and alarm call repertoire size additionally differs between females and males but it remains unclear if this corresponds to similar sexual dimorphisms in alarm calling strategies. We here experimentally investigated whether general female and more context-specific male alarm calls in putty-nosed monkeys ( Cercopithecus nictitans ) had different effects on the opposite sex's behaviour and whether they might serve different female and male alarm calling strategies. We presented a leopard model separately to the females or to the male of several groups while ensuring that the opposite sex only heard alarm calls of target individuals. While female alarms led to the recruitment of males in the majority of cases, male alarms did not have a similar effect on female behaviour. Males further seem to vocally advertise their engagement in group defence with more unspecific alarms while approaching their group. Males switched alarm call types once they spotted the leopard model and started mobbing behaviour. Females only ceased to alarm call when males produced calls typically associated with anti-predator defence, but not when males produced unspecific alarm calls. Our results suggest that sexual dimorphisms in the context specificity of alarms most likely correspond to different alarm calling strategies in female and male putty-nosed monkeys.