Predator‐Associated Vocalizations in North American Red Squirrels (Tamiasciurus hudsonicus): To Whom are Alarm Calls Addressed and How do They Function?

Alarm vocalizations produced by prey species encountering predators can serve a variety of functions. North American red squirrels are a small-bodied mammal popularly known for producing loud, conspicuous alarm calls, but functional accounts of calling in this species are few and contradictory. We conducted research over a 3-yr period on a sample of 47 marked red squirrels in the foothills of the Canadian Rockies. We recorded the production of alarm calls during encounters with natural predators and in a series of simulated predator experiments. We tested for variation in call production patterns consistent with three traditional hypotheses concerning the conspecific warning functions of alarm calling: namely that they serve as warnings to kin, to potential mates, or to territorial neighbors with which callers have an established relationship. Patterns of calling did not provide clear support for any of these hypothesized functions. We consider several possible qualifications to our results. We also consider the possibility that conspicuous calls given by red squirrels during encounters with predators are directed at the predators themselves and function to announce their detection and possibly deter them. This possibility is consistent with additional life-history features of red squirrels including that they are a relatively solitary and territorial, food-hoarding species that produces the same conspicuous vocalizations in response to other squirrels intruding on their territory to steal cones. An important corollary of this account is that red squirrel alarm calls probably do not entail referentially specific messages about different types of predator, as proposed previously.     

Contact calls of common marmosets (Callithrix jacchus): influence of age of caller on antiphonal calling and other vocal responses

Marmosets, as do many other primates, live in forest environments, are group living and constantly at risk of predation. Retaining contact with one another is therefore a matter of survival. We ask here whether their contact calls (phee and twitter vocalizations) are in some way ordered acoustically by sex or age and whether the calls of older marmosets elicit different responses than those of younger marmosets. In our study, marmosets (2–14 years) were visually isolated from conspecifics and the vocal responses to each isolated caller by other marmosets in the colony were recorded. Vocal responses to phee calls largely consisted of phee calls and, less commonly, twitter calls. No differences between the responses to calls by males and females were apparent. However, we found a strong positive and significant correlation between the caller's age and the percentage of its phee calls receiving a phee response, and a significant negative correlation between the caller's age and the percentage of its phee calls receiving a twitter response. The older the marmoset, the more antiphonal calling occurred. Two‐syllable phee calls were emitted more often by older marmosets (10–14 years) than by younger ones (2–6 years). Hence, we have found age‐dependent differences in phee‐call production and a consistent change in the response received across the adult life‐span. This age‐dependent effect was independent of kinship relations. This is the first evidence that marmosets distinguish age by vocal parameters alone and make social decisions based on age. Am. J. Primatol. 71:165–170, 2009. © 2008 Wiley‐Liss, Inc.     

From nestling calls to fledgling silence: adaptive timing of change in response to aerial alarm calls

Young birds and mammals are extremely vulnerable to predators and so should benefit from responding to parental alarm calls warning of danger. However, young often respond differently from adults. This difference may reflect: (i) an imperfect stage in the gradual development of adult behaviour or (ii) an adaptation to different vulnerability. Altricial birds provide an excellent model to test for adaptive changes with age in response to alarm calls, because fledglings are vulnerable to a different range of predators than nestlings. For example, a flying hawk is irrelevant to a nestling in a enclosed nest, but is dangerous to that individual once it has left the nest, so we predict that young develop a response to aerial alarm calls to coincide with fledging. Supporting our prediction, recently fledged white-browed scrubwrens, Sericornis frontalis, fell silent immediately after playback of their parents' aerial alarm call, whereas nestlings continued to calling despite hearing the playback. Young scrubwrens are therefore exquisitely adapted to the changing risks faced during development.     

Calling at a cost: elevated nestling calling attracts predators to active nests

Begging by nestling birds has been used to test evolutionary models of signalling but theory has outstripped evidence. Eavesdropping predators potentially impose a cost on begging that ensures signal honesty, yet little experimental evidence exists for such a cost at active nests because the use of artificial nests, long playback bouts and absence of parents may have exaggerated costs. We broadcast short periods (1 h) of either nestling vocalizations or background noise at active white-browed scrubwren, Sericornis frontalis, nests. Nestlings called naturally during both treatments, allowing us to test whether elevated calling increases risk, a key but rarely tested assumption of evolutionary models. Predators visited nests exclusively during periods of elevated calling. Furthermore, playbacks affected neither adult visits nor nestling activity, suggesting that calling alone attracted predators. Adults gave alarm calls and nestlings usually called less when predators approached nests. Predation risk to broods is, therefore, likely to fluctuate substantially over short periods of time, depending on nestling hunger and whether adults or young have detected predators. This study confirms a present-day cost of nestling begging, demonstrates that this cost can be incurred over short periods and supports the importance of parent-offspring antipredator strategies in reducing predation risk.     

Nest defence in the American goldfinch

In the American goldfinch (Carduelis tristis), vocalizations during nest defence consist largely of two different types of calls: either ‘sweeet’ (SWT) or ‘bearbee’ (BB). By recording call rates and behaviour during controlled experiments, it was demonstrated that: (1) SWT calls have a rallying function and attract more goldfinches than BB calls; (2) goldfinches attempt to distract potential predators away from their nests; (3) BB calls cause a decrease in nestling conspicuousness, both audibly and visually; (4) call rates show a positive relationship with increasing conspicuousness of nestlings; (5) call rates of BB and SWT calls vary inversely with danger to the nest; (6) high call rates are given by parents with successful nests whereas low call rates are associated with failures caused by nest predation; (7) call rates show a positive relationship with clutch and brood size; (8) call rates and types did not vary with different potential predators; and (9) call rates and types used by males and females are related to their respective roles in the nesting cycle. Several hypotheses are discussed that might explain changes in call rates through the nesting cycle.     

The versatility of graded acoustic measures in classification of predation threats by the tufted titmouse Baeolophus bicolor: exploring a mixed framework for threat communication

Many mammal and bird species respond to predator encounters with alarm vocalizations that generate risk‐appropriate responses in listeners. Two conceptual frameworks are typically applied to the information encoded in alarm calls and to associated anti‐predator behaviors. ‘Functionally referential’ alarm systems encode nominal classes or categories of risk in distinct call types that refer to distinct predation‐risk situations. ‘Risk‐based’ alarms encode graded or ranked threat‐levels by varying the production patterns of the same call types as the urgency of predation threat changes. Recent work suggests that viewing alarm‐response interactions as either referential or risk‐based may oversimplify how animals use information in decision‐making. Specifically, we explore whether graded alarm cues may be useful in classifying risks, supporting a referential decision‐making framework. We presented predator (hawk, owl, cat, snake) and control treatments to captive adult tufted titmice Baeolophus bicolor and recorded their vocalizations, which included ‘chick‐a‐dee’ mobbing calls (composed of chick and D notes), ‘seet’ notes, two types of contact notes (‘chip’, ‘chink’), and song. No single call type was uniquely associated with any treatment and the majority of acoustic measures varied significantly among treatments (46 of 60). The strongest models (ANOVA and classification tree analysis) grouped hawk with cat and owl, and control with snake, and were based on the number or proportion of a) chick and D notes per chick‐a‐dee call, b) chip versus chink notes produced following treatment exposure, and c) the frequency metrics of other note types. We conclude that (1) the predation‐threat information available in complex titmouse alarm calls was largely encoded in graded acoustic measures that were (2) numerous and variable across treatments and (3) could be used singly or in combinations for either ranking or classification of threats. We call attention to the potential use of mixed threat identification strategies, where risk‐based signal information may be used in referential decision‐making contexts.     

Begging and the risk of predation in nestling birds

Theoretical models of the evolution of begging in nestling passerinesassume that begging is costly, either energetically or in termsof predation. However, few empirical measures of these costsexist. We examined whether nestling begging calls could attractpredators to nests by comparing predation rates at artificialnests with and without playbacks of tree swallow begging calls.Nests were baited with quail eggs and placed in pairs on theground or in modified nest-boxes. Nests with playbacks of beggingcalls were depredated before control nests significantly moreoften in both the ground and nest-box trials, suggesting thatpredators may use begging calls to locate nests. These resultssuggest that the risk of nest predation may be increased becauseof calling by nestlings and provide further support for theassumption that conspicuous begging is costly in terms of predation     

VOCAL REPERTOIRE OF WILD BREEDING ORANGE-WINGED PARROTS AMAZONA AMAZONICA IN AMAZONIA

ABSTRACT

The vocal repertoire of Amazona amazonica during its breeding season has been recorded from wild individuals in Santa Bárbara do Pará, Pará State, Brazil. At individual nests, we continuously recorded vocalizations and behaviour for four hours in the early morning and three hours in the late afternoon, three times a week throughout the breeding season. We identified nine vocalizations that we classified in three behavioural categories: (1) Flight call—emitted when parrots arrive in the nest area; (2) Perched contact calls—two different vocalizations, one of them related to feeding, were emitted when the pair was perched in the nest area and interacted socially between themselves or with other individuals; (3) Aggressive calls—emitted when birds were in a dangerous situation, i.e. alarm (three types of calls), agonistic contact and distress calls (two types of call). The Orange-winged Parrot is a highly social species and the complexity of its social interactions is reflected in the diversity of its vocal repertoire.     

Kea Nestor notabilis mothers produce nest-specific calls with low amplitude and high entropy

Vocal behaviour of nesting altricial birds is subject to selection pressure from several sources. Offspring beg to attract parents’ attention, thus increasing the chances of being fed, but also increasing the chances of being detected by predators. Research on passerines has shown that parents may reduce the risk of nest predation by alarm calling to warn nestlings to be quiet, and by producing food calls which solicit begging when parents are present to defend the nestlings. Both nestlings and parents may reduce the risk of predator detection by producing calls of low amplitude and high entropy which are acoustically difficult to locate. Although extensive research has been undertaken on nesting passerine vocalizations, little is known about parrots in this regard, and studies are needed to determine whether parrots show similar adaptations. We investigated the calling behaviour of Kea Nestor notabilis mothers during the nesting period to determine whether maternal vocalizations were adapted in a way that could increase the chance of brood success. A microphone was installed inside the nest to record calls produced both inside the nest and in the direct vicinity. Our prediction was that calls outside the nest would be easy to locate and could function as alarm calls to alert conspecifics or distract the predator, whereas calls inside the nest would be difficult to locate and could serve to communicate with nestlings without alerting predators. Our results accorded with these predictions. Calls produced outside the nest were loud and tonal, and corresponded to previously described Kea alarm calls. Calls produced inside the nest, however, were high-entropy and low-amplitude calls, and formed a distinct structural category. We thus provide the first evidence that a parrot species has a vocal category for communication inside the nest, and that calls within this category are structured in a way that could reduce the risk of nest predation.     

Evidence of selection for egg crypsis in conspicuous nests

ABSTRACT The value of egg coloration as crypsis, once accepted as a general principle, has recently been questioned because most experiments have failed to show that egg coloration deters predation. The nest‐crypsis hypothesis postulates that, among species that build conspicuous nests, selection for egg crypsis is relaxed or absent because visually searching predators detect nests prior to eggs. I tested the nest‐crypsis hypothesis using the large, relatively conspicuous nests of American Robins (Turdus migratorius), and eggs that differed markedly in color that were collected from the nests of Red‐winged Blackbirds (Agelaius phoeniceus), Brewer's Blackbirds (Euphagus cyanocephalus), and Yellow‐headed Blackbirds (Xanthocephalus xanthocephalus). Each nest (N= 22) received a clutch of each species during three sequential predation trials that were 16 d in duration. The order of clutch presentation was randomized for each nest. Survival trends for Brewer's and Yellow‐headed Blackbirds were similar, and higher than those for clutches of Red‐winged Blackbirds. By the end of trials, overall survival of the three clutch types was roughly equivalent. However, clutches of Red‐winged Blackbird eggs, the most conspicuous egg type to the human eye, were discovered sooner by predators. Because the experimental design controlled for effects of nest crypsis, nest location, and nest size, this difference in egg survival can be attributed to differences in egg pigmentation. Thus, my results support a role for egg coloration as camouflage in conspicuous nests.     

Effect of alarm calling by male Red‐winged Blackbirds on nestling begging and female provisioning behavior

ABSTRACT Nestling begging and parental provisioning can attract nest predators and reduce reproductive success, so parents and their offspring might be expected to respond adaptively by minimizing predator‐attracting cues when predators threaten nests. Male Red‐winged Blackbirds (Agelaius phoeniceus) are well known for their antipredator alarm calls that contain information about the approach of potential nest predators. We examined the begging behavior of nestlings and the provisioning behavior of females in response to antipredator alarm calls of males to test the adaptive response hypothesis. Playback experiments provided no evidence that alarm calls function to switch off vocal begging; nestlings were equally likely to beg vocally during playback and control periods. Video recordings showed that male alarm calling had no significant effect on inappropriate vocal begging (in the absence of an adult), but significantly reduced the incidence of spontaneous calling (in the absence of begging). Adult females responded to male antipredator alarm calls by delaying their provisioning visits. In addition, although having no significant effect on use of nest‐arriving calls by females, male alarm calling significantly reduced their use of nest‐leaving calls. We conclude that nestling and female Red‐winged Blackbirds respond to male alarm calls in ways that might reduce the risk of predation, but nestlings beg vocally when females arrive to feed them, regardless of male alarm calling, perhaps to avoid a competitive disadvantage with broodmates.     

Asymmetrical interspecific communication of predatory threat in mixed‐species colonies of lesser kestrels (Falco naumanni) and jackdaws (Corvus monedula)

Sympatric species derive benefits by attending to information conveyed by heterospecifics. Our previous finding of reduced vigilance among jackdaws and lesser kestrels residing in mixed‐species colonies suggested a reliance on interspecific communication of information regarding predatory threats. To test for interspecific communication of threat, we first determined whether jackdaw and lesser kestrel call structure varied with perceived threat. In this call production phase of our study, free‐living birds in mixed‐species colonies were presented with models representing a potential nest predator (European magpie) or with non‐threatening stimuli (wood pigeon or wooden dowel) in proximity to nests. We recorded and subsequently analysed those calls to determine if any temporal or frequency‐related call parameters differed by model type. In a second, perceptual phase of our study, we tested whether receivers perceive threat‐related variation in both conspecific and heterospecific call structure by playing back call exemplars recorded in response to the predator model or to innocuous control stimuli, to determine whether free‐living jackdaws or lesser kestrels respond differentially to playbacks of the different call types. We detected differences in vocalizations of both jackdaws and lesser kestrels relative to the model type presented, with more broadband (lesser kestrel) or noisy calls (jackdaws) in response to magpie versus innocuous model types. We also detected differential behavioural responses to call playbacks, with both jackdaws and lesser kestrels increasing vigilance and alarm calling in response to magpie‐elicited jackdaw calls, but not to other call types. Taken together, our results suggest that jackdaw, but not lesser kestrel vocalizations, communicate enhanced threat associated with European magpies as possible nest predators. This interspecific alarm communication benefits both jackdaws and lesser kestrels, and, at least in part, explains asymmetric responses of jackdaws and lesser kestrels to magpies attending mixed‐species colonies in nature.     

Responses of naive yellow warblers to a novel nest predator

Naive parental yellow warblers, Dendroica petechia, were tested with a mounted eastern grey squirrel, Sciurus carolinensis, a novel predator on the study site, during the nest-building, egg-laying, incubation and nestling stages of the nesting cycle. Testing parents only once avoided the possibility that the nest defence behaviour of the parents was modified by reinforcement and loss of fear. In 96% of 80 trials, the female parent responded first to the model. Males rarely showed nest defence behaviour. Female nest defence as measured by defensive vocalizations (i.e., ‘chipping’), closest and modal distance of approach to the model, distraction displays, strikes, and close passes or hovers, did not increase significantly over the breeding season. ‘Chipping’ frequency by both sexes tended to increase after the incubation period but not significantly so. Distraction displays increased significantly only between nest-building and nestling stages. Age, clutch or brood size, and nest success were not correlated with the intensity of nest defence. Females defending exposed nests gave more distraction displays than those defending cryptic nests.     

Influence of nests of leaf‐cutting ants on plant species diversity in road verges of northern Patagonia

Abstract. It has been suggested that ant nests are the most frequent small‐scale disturbance that affect vegetation patterns. However, their effects on plant diversity are little studied. We document effects of nests of the leaf‐cutting ant Acromyrmex lobicornis on physical‐chemical soil properties and their influence on plant diversity near road verges in a desert steppe in NW Patagonia, Argentina. We analysed nest soils and controls for nitrogen, phosphorus, organic matter, moisture retention capacity and texture. We also analysed the vegetation on 42 nests (30 active and 12 abandoned or without life) and 42 areas without nests. Soil around nests had a greater nutrient content and capacity to retain moisture than control soils, which is mainly due to the presence of organic waste that the ants deposit on the soil surface. We found no association between the occurrence of nests and specific groups of plants, but plant diversity was higher at nest‐sites than at nearby non‐nest sites. This increased diversity – which is also found on abandoned nests – is mainly due to the occurrence of a larger number of native and exotic plant species on nest‐sites that are uncommon elsewhere in the study area. The most abundant plant species showed similar cover values at nest and non‐nest sites. This suggests that changes in diversity are associated to edaphic changes caused by nests rather than by changes in competitive balance caused by dominant species exclusion. We propose that the nests of Acromyrmex lobicornis, through increasing the availability of resources, generate favourable microsites that can function both as ‘refuges’ for less frequent native species, and as‘stepping stones’ for less frequent exotic plant species.     

Buildings promote higher incubation temperatures and reduce nest attentiveness in a Neotropical thrush

Incubation is an energetically costly parental task of breeding birds. Incubating parents respond to environmental variation and nest‐site features to adjust the balance between the time spent incubating (i.e. nest attentiveness) and foraging to supply their own needs. Non‐natural nesting substrates such as human buildings impose new environmental contexts that may affect time allocation of incubating birds but this topic remains little studied. Here, we tested whether nesting substrate type (buildings vs. trees) affects the temperature inside the incubation chamber (hereafter ‘nest temperature’) in the Pale‐breasted Thrush Turdus leucomelas, either during ‘day’ (with incubation recesses) or ‘night’ periods (representing uninterrupted female presence at the nest). We also tested whether nesting substrate type affects the incubation time budget using air temperature and the day of the incubation cycle as covariates. Nest temperature, when controlled for microhabitat temperature, was higher at night and in nests in buildings but did not differ between daytime and night for nests in buildings, indicating that buildings partially compensate for incubation recesses by females with regard to nest temperature stability. Females from nests placed in buildings exhibited lower nest attentiveness (the overall percentage of time spent incubating) and had longer bouts off the nest. Higher air temperatures were significantly correlated with shorter bouts on the nest and longer bouts off the nest, but without affecting nest attentiveness. We suggest that the longer bouts off the nest taken by females of nests in buildings is a consequence of higher nest temperatures promoted by man‐made structures around these nests. Use of buildings as nesting substrate may therefore increase parental fitness due to a relaxed incubation budget, and potentially drive the evolution of incubation behaviour in certain urban bird populations.     

Intended Receivers and Functional Significance of Grunt and Girney Vocalizations in Free-Ranging Female Rhesus Macaques

We investigated the intended receivers and contexts of occurrence of grunt and girney vocalizations in rhesus macaques (Macaca mulatta) to assess whether these calls are best interpreted as signals of benign intent or as calls that may function to attract the attention of other individuals or induce arousal. We focally observed 19 free‐ranging adult female rhesus macaques. Female calls increased dramatically after infants were born, and most were directed toward mother–infant dyads. When infants were physically separated from their mothers, callers visually oriented toward infants in over 90% of the cases, suggesting that infants were the intended receivers of grunts and girneys. Approaches followed by vocalizations were more likely to lead to the caller grooming the mother, less likely to elicit a submissive response, and more likely to result in infant handling than approaches without calls. Infant handling, however, was not necessarily benign. Vocalizations were often emitted from a distance >1 m and were rarely followed by approaches or social interactions. Our results suggest that grunts and girneys are unlikely to have evolved as signals that encode information about the caller's intention or subsequent behavior. Whereas girneys may be acoustically designed to attract infants’ attention and elicit arousal, grunts may have no adaptive communicative function. Mothers, however, may have learned that other females’ grunts and girneys are unlikely to be associated with significant risk and, therefore, are generally tolerant of the caller's proximity and behavior.     

Influence of Nest Deprivation on Behaviour,Hormonal Concentrations and on the Ability to Resume Incubation in Domestic Hens (Gallus domesticus)

In this study, we investigated the influence of the length of nest deprivation period (3 vs. 6 d) on the ability to renest of incubating hens. We focused on the hens' behaviour, particularly on nesting and calls, on their prolactin, luteinizing hormone (LH) and oestradiol concentrations. Nest deprivation induced a drop of prolactin and an increase of LH plasmatic concentrations in hens. These changes in circulating pituitary hormones were followed by changes in ovarian function: the persistent rise of plasmatic oestradiol gave evidence of the resumption of ovarian activity. After nest deprivation, the number of clucks increased significantly and food calls appeared; these results demonstrate that ‘maternal’ calls can be emitted outside the maternal context. Our results suggest that the onset of typical maternal calling is strongly controlled by internal state such as plasmatic hormonal concentrations, independently of social stimulation. None of the 10 hens deprived for 6 d resumed incubation when given the opportunity, whereas, after a 3 d deprivation period, three out of 10 hens renested and two hens incubated sporadically and then gradually abandoned their nests. Long periods of nest deprivation appear to disrupt the habits of sitting and nesting. Before nest reopening, all the hens presented low levels of plasmatic prolactin. Plasma prolactin concentrations of the renesting hens increased after nest boxes were reopened and returned to levels found in incubating hens. We suggest that pituitary prolactin rather than plasmatic prolactin is responsible for the maintenance of incubating potential in hens deprived of their nests.     

Testing hypotheses about the function of repeated nest abandonment as a life history strategy in a passerine bird

Nest structures are essential for successful reproduction in most bird species. Nest construction costs time and energy, and most bird species typically build one nest per breeding attempt. Some species, however, build more than one nest, and the reason for this behaviour is often unclear. In the Grey Fantail Rhipidura albiscapa, nest abandonment before egg‐laying is very common. Fantails will build up to seven nests within a breeding season, and pairs abandon up to 71% of their nests before egg‐laying. We describe multiple nest‐building behaviour in the Grey Fantail and test four hypotheses explaining nest abandonment in this species: cryptic depredation, destruction of nests during storm events, and two anti‐predatory responses (construction of decoy nests to confuse predators, and increasing concealment to ‘hide’ nests more effectively). We found support for only one hypothesis – that abandonment is related to nest concealment. Abandoned nests were significantly less concealed than nests that received eggs. Most abandoned nests were not completely built and none received eggs, thus ruling out cryptic predation. Nests were not more likely to be abandoned following storm events. The decoy nest hypothesis was refuted as abandoned nests were constructed at any point during the breeding season and some nests were dismantled and the material used to build the subsequent nest. Thus, Grey Fantails are flexible about nest‐site locations during the nest‐building phase and readily abandon nest locations if they are found to have deficient security.     

Group Mobbing Behaviour and Nest Defence in a Cooperatively Breeding Australian Bird

Cooperatively breeding noisy miners (Manorina melanocephala) are well known in Australia for their persistent and very vocal group mobbing of heterospecifics. Here I investigated the nature of this extraordinary behaviour, in particular its role in nest defence, in a colour banded population of noisy miners in south‐east Queensland, Australia. I focused on two questions. First, did the intensity of mobbing vary according to factors such as the threat to the nest, or the ‘value’ of a clutch? Secondly, what role did group mobbing play in the success of a nest? To answer these questions, I experimentally manipulated the nest defence behaviour by placing one of three stuffed models near active noisy miner nests. The response of noisy miners to intruders was not indiscriminate. However, I found that the number of birds that mobbed a model did not simply reflect the potential threat posed. The response of noisy miners to raptors and other potential nest predators may have reflected their rarity as well as the threat posed. The number of mobbers did not vary with the age or size of a brood. In this study, the fate of nests was independent of the number of mobbers or visitors at nests. Finally, up to 80% of mobbers were never seen to make any other type of contribution to a nest, and many could not be related to the brood that they were ‘defending’. Hence, for some noisy miner ‘helpers’ the benefits that they accrued were probably not wholly dependent on the survival of the broods. I suggest that, in this gregarious species, mobbing behaviour at the nest may be a display of social status or individual quality. This hypothesis warrants further investigation.