Justin A. Welbergen

Climate change and the effects of temperature extremes on Australian flying-foxes

Little is known about the effects of temperature extremes on natural systems. This is of increasing concern now that climate models predict dramatic increases in the intensity, duration and frequency of such extremes. Here we examine the effects of temperature extremes on behaviour and demography of vulnerable wild flying-foxes (Pteropus spp.). On 12 January 2002 in New South Wales, Australia, temperatures exceeding 42°C killed over 3500 individuals in nine mixed-species colonies. In one colony, we recorded a predictable sequence of thermoregulatory behaviours (wing-fanning, shade-seeking, panting and saliva-spreading, respectively) and witnessed how 5–6% of bats died from hyperthermia. Mortality was greater among the tropical black flying-fox, Pteropus alecto (10–13%) than the temperate grey-headed flying-fox, Pteropus poliocephalus (less than 1%), and young and adult females were more affected than adult males (young, 23–49%; females, 10–15%; males, less than 3%). Since 1994, over 30 000 flying-foxes (including at least 24 500 P. poliocephalus) were killed during 19 similar events. Although P. alecto was relatively less affected, it is currently expanding its range into the more variable temperature envelope of P. poliocephalus, which increases the likelihood of die-offs occurring in this species. Temperature extremes are important additional threats to Australian flying-foxes and the ecosystem services they provide, and we recommend close monitoring of colonies where temperatures exceeding 42.0°C are predicted. The effects of temperature extremes on flying-foxes highlight the complex implications of climate change for behaviour, demography and species survival.

Social Transmission of a Host Defense Against Cuckoo Parasitism

Defeating the Cuckoo Brood parasite-host interactions show ongoing antagonistic coevolution. What mediates rapid behavioral changes that do not reflect genetic change? Davies and Welbergen (p. 1318) show that reed warblers learn from their neighbors to behave aggressively toward models of the parasitic common cuckoo. Furthermore, reed warblers seem to be predisposed to learn to respond to cuckoos as enemies: Hosts that witnessed neighbors mobbing a harmless parrot model did not increase their aggression toward a cuckoo model. Thus, birds have templates for threats, and relevant antithreat behaviors can be turned on or off depending on social experience. Social learning and predisposition explains why reed warblers mob parasitic cuckoos but not innocuous parrots. Coevolutionary arms races between brood parasites and hosts involve genetic adaptations and counter-adaptations. However, hosts sometimes acquire defenses too rapidly to reflect genetic change. Our field experiments show that observation of cuckoo (Cuculus canorus) mobbing by neighbors on adjacent territories induced reed warblers (Acrocephalus scirpaceus) to increase the mobbing of cuckoos but not of parrots (a harmless control) on their own territory. In contrast, observation of neighbors mobbing parrots had no effect on reed warblers’ responses to either cuckoos or parrots. These results indicate that social learning provides a mechanism by which hosts rapidly increase their nest defense against brood parasites. Such enemy-specific social transmission enables hosts to track fine-scale spatiotemporal variation in parasitism and may influence the coevolutionary trajectories and population dynamics of brood parasites and hosts.

Reed warblers discriminate cuckoos from sparrowhawks with graded alarm signals that attract mates and neighbours

Brood parasites and predators pose unique threats that may favour the evolution of enemy-specific defence strategies. We considered whether reed warblers, Acrocephalus scirpaceus, have a specific alarm call for common cuckoos, Cuculus canorus, and whether their alarms attract mates and neighbours. Mounts of cuckoos (threat to nest but harmless to adults) were significantly more likely to be mobbed and were mobbed more strongly, with rasp calls and mandible snaps, than mounts of sparrowhawks, Accipiter nisus (threat to adults only), or teal, Anas crecca (a harmless control). However, calls were not acoustically specific to the kind of enemy presented, but rather varied in usage with mount distance from the nest and mount species. This suggests that reed warbler alarm signals are not functionally referential, but rather convey immediacy of threat to the nest. Mates and neighbours often approached during calling, and playback experiments confirmed they were more likely to be attracted by mobbing calls than by control calls. The response was graded, with higher repetition rates of mobbing calls attracting more individuals. Nevertheless, it is unlikely that mobbing calls functioned solely to attract mates and neighbours because calling continued even after these were attracted and was not more likely when there were close neighbouring nests, and attracted neighbours were sometimes chased away by residents. Our results show that reed warblers discriminate a brood parasite from both a dangerous species and an innocuous species by using graded alarm signals that attract conspecifics. This is compatible with the idea that nest defence by reed warblers includes a specific evolved response to brood parasitism.

Cuckoo–hawk mimicry? An experimental test

The similarity between many Old World parasitic cuckoos (Cuculinae) and Accipiter hawks, in size, shape and plumage, has been noted since ancient times. In particular, hawk-like underpart barring is more prevalent in parasitic than in non-parasitic cuckoos. Cuckoo–hawk resemblance may reflect convergent evolution of cryptic plumage that reduces detection by hosts and prey, or evolved mimicry of hawks by parasitic cuckoos, either for protection against hawk attacks or to facilitate brood parasitism by influencing host behaviour. Here, we provide the first evidence that some small birds respond to common cuckoos Cuculus canorus as if they were sparrowhawks Accipiter nisus. Great tits and blue tits were equally alarmed and reduced attendance at feeders during and after the presentation of mounted specimens of common cuckoos and sparrowhawks, but not in response to control presentations of collared doves or teal. Plumage manipulations revealed that the strong alarm response to cuckoos depended on their resemblance to hawks; cuckoos with barred underparts were treated like hawks, while those with unbarred underparts were treated like doves. However, barring was not the only feature inducing alarm because tits showed similarly strong alarm to barred and unbarred hawks, and little alarm to barred doves. These responses of tits, unsuitable as hosts and hence with no history of cuckoo parasitism, suggest that naive small birds can mistake cuckoos for hawks. Thus, any cuckoo–hawk discrimination by host species is likely to be an evolved response to brood parasitism.

The capacity of refugia for conservation planning under climate change

Refugia – areas that may facilitate the persistence of species during large-scale, long-term climatic change –are increasingly important for conservation planning. There are many methods for identifying refugia, but the ability to quantify their potential for facilitating species persistence (ie their “capacity”) remains elusive. We propose a flexible framework for prioritizing future refugia, based on their capacity. This framework can be applied through various modeling approaches and consists of three steps: (1) definition of scope, scale, and resolution; (2) identification and quantification; and (3) prioritization for conservation. Capacity is quantified by multiple indicators, including environmental stability, microclimatic heterogeneity, size, and accessibility of the refugium. Using an integrated, semi-mechanistic modeling technique, we illustrate how this approach can be implemented to identify refugia for the plant diversity of Tasmania, Australia. The highest-capacity climate-change refugia we...

Timing of the evening emergence from day roosts of the grey-headed flying fox, Pteropus poliocephalus : the effects of predation risk, foraging needs, and social context

This study addresses the functional question of how variation in foraging strategy, predation risk, and social context influence the timing of the evening emergence from day roosts of the grey-headed flying fox, Pteropus poliocephalus. The onset of evening emergence was expected to vary according to the relative costs and benefits of emerging early and should, therefore, reflect an optimal trade-off between predation risks and foraging needs. The onset of the colony-wide emergence was closely correlated with the time of sunset and cloud cover. However, as expected, the onset of the colony-wide emergence was delayed when a diurnal avian predator was present, whereas the onset was advanced during lactation when presumably energetic demands are higher. The trade-off between predation risks and foraging needs was further reflected in the emergence times of individual bats: adult females emerged earlier when they had higher foraging needs as indicated by their body condition; young emerged later when they were smaller and likely to be more at risk from predation due to their less developed flying skills. However, the emergence time of adult males depended on their social status: smaller bachelor males emerged from the colony earlier than larger harem-holding males who guard their harems until the last female had left. Thus, whereas the colony-wide emergence time reflected the outcome of a trade-off between predation risks and general foraging needs, on an individual level, the outcome of this trade-off depended on sex, age, body condition, and structural size and was modified by social context.

Avian vocal mimicry: a unified conceptual framework

Mimicry is a classical example of adaptive signal design. Here, we review the current state of research into vocal mimicry in birds. Avian vocal mimicry is a conspicuous and often spectacular form of animal communication, occurring in many distantly related species. However, the proximate and ultimate causes of vocal mimicry are poorly understood. In the first part of this review, we argue that progress has been impeded by conceptual confusion over what constitutes vocal mimicry. We propose a modified version of Vane‐Wrights (1980) widely used definition of mimicry. According to our definition, a vocalisation is mimetic if the behaviour of the receiver changes after perceiving the acoustic resemblance between the mimic and the model, and the behavioural change confers a selective advantage on the mimic. Mimicry is therefore specifically a functional concept where the resemblance between heterospecific sounds is a target of selection. It is distinct from other forms of vocal resemblance including those that are the result of chance or common ancestry, and those that have emerged as a by‐product of other processes such as ecological convergence and selection for large song‐type repertoires. Thus, our definition provides a general and functionally coherent framework for determining what constitutes vocal mimicry, and takes account of the diversity of vocalisations that incorporate heterospecific sounds. In the second part we assess and revise hypotheses for the evolution of avian vocal mimicry in the light of our new definition. Most of the current evidence is anecdotal, but the diverse contexts and acoustic structures of putative vocal mimicry suggest that mimicry has multiple functions across and within species. There is strong experimental evidence that vocal mimicry can be deceptive, and can facilitate parasitic interactions. There is also increasing support for the use of vocal mimicry in predator defence, although the mechanisms are unclear. Less progress has been made in explaining why many birds incorporate heterospecific sounds into their sexual displays, and in determining whether these vocalisations are functionally mimetic or by‐products of sexual selection for other traits such as repertoire size. Overall, this discussion reveals a more central role for vocal mimicry in the behavioural ecology of birds than has previously been appreciated. The final part of this review identifies important areas for future research. Detailed empirical data are needed on individual species, including on the structure of mimetic signals, the contexts in which mimicry is produced, how mimicry is acquired, and the ecological relationships between mimic, model and receiver. At present, there is little information and no consensus about the various costs of vocal mimicry for the protagonists in the mimicry complex. The diversity and complexity of vocal mimicry in birds raises important questions for the study of animal communication and challenges our view of the nature of mimicry itself. Therefore, a better understanding of avian vocal mimicry is essential if we are to account fully for the diversity of animal signals.

Spatio-temporal vigilance architecture of an Australian flying-fox colony

The social structure of animal aggregations may vary considerably in both space and time, yet little is known about how this affects vigilance. Here, we investigate the vigilance architecture of a colony of wild-living grey-headed flying-foxes (Pteropus poliocephalus) in Australia and examine how spatial as well as temporal variation in social organization influences social and environmental vigilance. We sampled color-marked individuals at different stages of the reproductive cycle and the year and at different locations in the colony to examine the effects of temporal and spatial factors on social and environmental vigilance. We found that vigilance architecture reflected the social structure of the colony, with the highest environmental vigilance being displayed by bats at the periphery of the colony, and the highest social vigilance by bats that roosted at intermediate distances from the colony’s edge. Furthermore, we found that vigilance levels reflected changes in reproductive state, with social vigilance increasing toward the mating season, particularly in males. Our findings show that spatial and temporal variation in social structure can have differential effects on social and environmental vigilance. This highlights the necessity to differentiate between functions of vigilance to understand fully vigilance architecture in aggregations of social animals.

Fit females and fat polygynous males: seasonal body mass changes in the grey-headed flying fox.

When females and males differ in their timing of maximum reproductive effort, this can result in sex-specific seasonal cycles in body mass. Such cycles are undoubtedly under strong selection, particularly in bats, where they affect flying ability. Flying foxes (Old World fruit bats, Pteropus spp.) are the largest mammals that can sustain powered flight and therefore face critical trade-offs in managing body reserves for reproduction, yet little is known about body mass dynamics in this group. I investigated body mass changes in relation to reproductive behaviour in a large colony of grey-headed flying foxes (Pteropus poliocephalus). In this polygynous mammal, females were predicted to maximise reproductive effort during lactation and males during the breeding season. As predicted, female body condition declined during the nursing period, but did not vary in relation to sexual activity. By contrast, males accumulated body reserves prior to the breeding season, but subsequently lost over 20% of their body mass on territory defence and courtship, and lost foraging opportunities as they also defended their day roost territories at night. Males in better condition had larger testes, particularly during territory establishment, prior to maximum sexual activity. Thus, the seasonality of female mass reflected the high metabolic load that lactation imposes on mothers. However, male mass followed a pattern akin to the “fatted male phenomenon”, which is commonly observed in large polygynous mammals with seasonal reproduction, but not in bats. This shows the importance of body reserves for reproduction in flying foxes, despite their severe constraints on body mass.

Mother guarding: how offspring may influence the extra-pair behaviour of their parents

In this paper we propose a novel form of social control of mate choice. Through mother guarding, offspring can help in protecting the paternity of their father by preventing their mother from engaging in extra-pair matings. We present a model that predicts the circumstances under which mothers should be selected to seek or avoid extra-pair matings, and existing offspring should be selected to prevent or promote such matings. In its simplest form, our model shows that offspring are selected to mother guard as long as the viability of extra-pair young is less than twice that of within-pair young; when the relative viability is greater, offspring are selected to promote extra-pair mating by their mother. If the existing offspring are not necessarily sired by their mothers social mate, then the potential for conflict is further reduced. We also consider whether offspring have an interest in the extra-pair reproduction of their fathers. We show that when the costs of the fathers infidelity to the mothers brood are high, existing offspring are selected to prevent extra-pair mating by their father; when such costs are low, offspring are selected to promote extra-pair mating by their father. In principle, our model applies to all species where offspring show delayed dispersal and where breeding pairs raise multiple broods or litters. This situation exists in, but is not limited to, the majority of cooperatively breeding species. The significance of this model with regard to our current understanding of the evolution of extra-pair behaviour in such species is discussed.