Human-modified landscapes provide key foraging areas for a threatened flying mammal: The grey-headed flying-fox.

Urban expansion is a major threat to natural ecosystems but also creates novel opportunities that adaptable species can exploit. The grey-headed flying-fox (Pteropus poliocephalus) is a threatened, highly mobile species of bat that is increasingly found in human-dominated landscapes, leading to many management and conservation challenges. Flying-fox urbanisation is thought to be a result of diminishing natural foraging habitat or increasing urban food resources, or both. However, little is known about landscape utilisation of flying-foxes in human-modified areas, and how this may differ in natural areas. Here we examine positional data from 98 satellite-tracked P. poliocephalus for up to 5 years in urban and non-urban environments, in relation to vegetation data and published indices of foraging habitat quality. Our findings indicate that human-modified foraging landscapes sustain a large proportion of the P. poliocephalus population year-round. When individuals roosted in non-urban and minor-urban areas, they relied primarily on wet and dry sclerophyll forest, forested wetlands, and rainforest for foraging, and preferentially visited foraging habitat designated as high-quality. However, our results highlight the importance of human-modified foraging habitats throughout the species' range, and particularly for individuals that roosted in major-urban environments. The exact plant species that exist in human-modified habitats are largely undocumented; however, where this information was available, foraging by P. poliocephalus was associated with different dominant plant species depending on whether individuals roosted in 'urban' or 'non-urban' areas. Overall, our results demonstrate clear differences in urban- and non-urban landscape utilisation by foraging P. poliocephalus. However, further research is needed to understand the exact foraging resources used, particularly in human-modified habitats, and hence what attracts flying-foxes to urban areas. Such information could be used to modify the urban foraging landscape, to assist long-term habitat management programs aimed at minimising human-wildlife conflict and maximising resource availability within and outside of urban environments.

Extreme mobility of the world's largest flying mammals creates key challenges for management and conservation.

BACKGROUND: Effective conservation management of highly mobile species depends upon detailed knowledge of movements of individuals across their range; yet, data are rarely available at appropriate spatiotemporal scales. Flying-foxes (Pteropus spp.) are large bats that forage by night on floral resources and rest by day in arboreal roosts that may contain colonies of many thousands of individuals. They are the largest mammals capable of powered flight, and are highly mobile, which makes them key seed and pollen dispersers in forest ecosystems. However, their mobility also facilitates transmission of zoonotic diseases and brings them in conflict with humans, and so they require a precarious balancing of conservation and management concerns throughout their Old World range. Here, we analyze the Australia-wide movements of 201 satellite-tracked individuals, providing unprecedented detail on the inter-roost movements of three flying-fox species: Pteropus alecto, P. poliocephalus, and P. scapulatus across jurisdictions over up to 5 years. RESULTS: Individuals were estimated to travel long distances annually among a network of 755 roosts (P. alecto, 1427-1887 km; P. poliocephalus, 2268-2564 km; and P. scapulatus, 3782-6073 km), but with little uniformity among their directions of travel. This indicates that flying-fox populations are composed of extremely mobile individuals that move nomadically and at species-specific rates. Individuals of all three species exhibited very low fidelity to roosts locally, resulting in very high estimated daily colony turnover rates (P. alecto, 11.9 ± 1.3%; P. poliocephalus, 17.5 ± 1.3%; and P. scapulatus, 36.4 ± 6.5%). This indicates that flying-fox roosts form nodes in a vast continental network of highly dynamic "staging posts" through which extremely mobile individuals travel far and wide across their species ranges. CONCLUSIONS: The extreme inter-roost mobility reported here demonstrates the extent of the ecological linkages that nomadic flying-foxes provide across Australia's contemporary fragmented landscape, with profound implications for the ecosystem services and zoonotic dynamics of flying-fox populations. In addition, the extreme mobility means that impacts from local management actions can readily reverberate across jurisdictions throughout the species ranges; therefore, local management actions need to be assessed with reference to actions elsewhere and hence require national coordination. These findings underscore the need for sound understanding of animal movement dynamics to support evidence-based, transboundary conservation and management policy, tailored to the unique movement ecologies of species.

Foraging enrichment alleviates oral repetitive behaviors in captive red-tailed black cockatoos (Calyptorhynchus banksii).

The relationship between inadequate foraging opportunities and the expression of oral repetitive behaviors has been well documented in many production animal species. However, this relationship has been less-well examined in zoo-housed animals, particularly avian species. The expression of oral repetitive behavior may embody a frustrated foraging response, and may therefore be alleviated with the provision of foraging enrichment. In this study, we examined the effect of different foraging-based enrichment items on a group of captive red-tailed black cockatoos who were previously observed performing oral repetitive behavior. A group of six cockatoos were presented with five foraging enrichment conditions (no enrichment (control), sliced cucumber, fresh grass, baffle cages, and millet discs). Baseline activity budgets were established over a 10-day preintervention period and interventions were then presented systematically over a 25-day experimental period. This study demonstrated that the provision of foraging interventions effectively increased the median percentage of time spent foraging compared to control conditions (range, 5.0-31.7% across interventions vs. 5.0% for control), with two of the interventions; grass and millet discs, significantly decreasing the expression of oral repetitive behaviors (control = 16.6 vs. 8.3% for both grass and millet discs). Finally, a rapid-scoring method utilized by zookeepers during the study proved to be a useful proxy for the amount of time the cockatoos spent interacting with the foraging interventions and overall time spent foraging.

Using weather radar to monitor the number, timing and directions of flying-foxes emerging from their roosts.

Knowledge of species' population trends is crucial when planning for conservation and management; however, this information can be difficult to obtain for extremely mobile species such as flying-foxes (Pteropus spp.; Chiroptera, Pteropodidae). In mainland Australia, flying-foxes are of particular management concern due their involvement in human-wildlife conflict, and their role as vectors of zoonotic diseases; and two species, the grey-headed flying-fox (Pteropus poliocephalus) and the spectacled flying-fox (P. conspicillatus), are currently threatened with extinction. Here we demonstrate that archival weather radar data over a period of ten years can be used to monitor a large colony of grey-headed flying-foxes near Melbourne. We show that radar estimates of colony size closely match those derived from traditional counting methods. Moreover, we show that radar data can be used to determine the timing and departure direction of flying-foxes emerging from the roost. Finally, we show that radar observations of flying-foxes can be used to identify signals of important ecological events, such as mass flowering and extreme heat events, and can inform human activities, e.g. the safe operation of airports and windfarms. As such, radar represents an extremely promising tool for the conservation and management of vulnerable flying-fox populations and for managing human interactions with these ecologically-important mammals.

Substantial reduction in thermo-suitable microhabitat for a rainforest marsupial under climate change.

Increases in mean temperatures caused by anthropogenic climate change increase the frequency and severity of temperature extremes. Although extreme temperature events are likely to become increasingly important drivers of species' response to climate change, the impacts are poorly understood owing mainly to a lack of understanding of species' physiological responses to extreme temperatures. The physiological response of Pseudochirops archeri (green ringtail possum) to temperature extremes has been well studied, demonstrating that heterothermy is used to reduce evaporative water loss at temperatures greater than 30°C. Dehydration is likely to limit survival when animals are exposed to a critical thermal regime of ≥30°C, for ≥5 h, for ≥4 consecutive days. In this study, we use this physiological information to assess P. archeri's vulnerability to climate change. We identify areas of current thermo-suitable habitat (validated using sightings), then estimate future thermo-suitable habitat for P. archeri, under four emission scenarios. Our projections indicate that up to 86% of thermo-suitable habitat could be lost by 2085, a serious conservation concern for the species. We demonstrate the potential applicability of our approach for generating spatio-temporally explicit predictions of the vulnerability of species to extreme temperature events, providing a focus for efficient and targeted conservation and habitat restoration management.

Landscape complexity influences route-memory formation in navigating pigeons.

Observations of the flight paths of pigeons navigating from familiar locations have shown that these birds are able to learn and subsequently follow habitual routes home. It has been suggested that navigation along these routes is based on the recognition of memorized visual landmarks. Previous research has identified the effect of landmarks on flight path structure, and thus the locations of potentially salient sites. Pigeons have also been observed to be particularly attracted to strong linear features in the landscape, such as roads and rivers. However, a more general understanding of the specific characteristics of the landscape that facilitate route learning has remained out of reach. In this study, we identify landscape complexity as a key predictor of the fidelity to the habitual route, and thus conclude that pigeons form route memories most strongly in regions where the landscape complexity is neither too great nor too low. Our results imply that pigeons process their visual environment on a characteristic spatial scale while navigating and can explain the different degrees of success in reproducing route learning in different geographical locations.

Homing pigeons respond to time-compensated solar cues even in sight of the loft.

The sun has long been thought to guide bird navigation as the second step in a two-stage process, in which determining position using a map is followed by course setting using a compass, both over unfamiliar and familiar terrain. The animal's endogenous clock time-compensates the solar compass for the sun's apparent movement throughout the day, and this allows predictable deflections in orientation to test for the compass' influence using clock-shift manipulations. To examine the influence of the solar compass during a highly familiar navigational task, 24 clock-shifted homing pigeons were precision-tracked from a release site close to and in sight of their final goal, the colony loft. The resulting trajectories displayed significant partial deflection from the loft direction as predicted by either fast or slow clock-shift treatments. The partial deflection was also found to be stable along the entire trajectory indicating regular updating of orientation via input from the solar compass throughout the final approach flight to the loft. Our results demonstrate that time-compensated solar cues are deeply embedded in the way birds orient during homing flight, are accessed throughout the journey and on a remarkably fine-grained scale, and may be combined effectively simultaneously with direct guidance from familiar landmarks, even when birds are flying towards a directly visible goal.

Ecological and demographic correlates of helping behaviour in a cooperatively breeding bird.

The evolution of cooperation is a persistent problem for evolutionary biologists. In particular, understanding of the factors that promote the expression of helping behaviour in cooperatively breeding species remains weak, presumably because of the diverse nature of ecological and demographic drivers that promote sociality. In this study, we use data from a long-term study of a facultative cooperative breeder, the long-tailed tit Aegithalos caudatus, to investigate the factors influencing annual variation in helping behaviour. Long-tailed tits exhibit redirected helping in which failed breeders may become helpers, usually at a relative's nest; thus, helping is hypothesised to be associated with causes of nest failure and opportunities to renest or help. We tested predictions regarding the relationship between annual measures of cooperative behaviour and four explanatory variables: nest predation rate, length of the breeding season, population-level relatedness and population density. We found that the degree of helping was determined principally by two factors that constrain successful independent reproduction. First, as predicted, cooperative behaviour peaked at intermediate levels of nest predation, when there are both failed breeders (i.e. potential helpers) and active nests (i.e. potential recipients) available. Second, there were more helpers in shorter breeding seasons when opportunities for renesting by failed breeders are more limited. These are novel drivers of helping behaviour in avian cooperative breeding systems, and this study illustrates the difficulty of identifying common ecological or demographic factors underlying the evolution of such systems.

An experimental test of the information model for negotiation of biparental care.

BACKGROUND: Theoretical modelling of biparental care suggests that it can be a stable strategy if parents partially compensate for changes in behaviour by their partners. In empirical studies, however, parents occasionally match rather than compensate for the actions of their partners. The recently proposed "information model" adds to the earlier theory by factoring in information on brood value and/or need into parental decision-making. This leads to a variety of predicted parental responses following a change in partner work-rate depending on the information available to parents. METHODOLOGY/PRINCIPAL FINDINGS: We experimentally test predictions of the information model using a population of long-tailed tits. We show that parental information on brood need varies systematically through the nestling period and use this variation to predict parental responses to an experimental increase in partner work-rate via playback of extra chick begging calls. When parental information is relatively high, partial compensation is predicted, whereas when parental information is low, a matching response is predicted. CONCLUSIONS/SIGNIFICANCE: We find that although some responses are consistent with predictions, parents match a change in their partner's work-rate more often than expected and we discuss possible explanations for our findings.

Objectively identifying landmark use and predicting flight trajectories of the homing pigeon using Gaussian processes.

Pigeons home along idiosyncratic habitual routes from familiar locations. It has been suggested that memorized visual landmarks underpin this route learning. However, the inability to experimentally alter the landscape on large scales has hindered the discovery of the particular features to which birds attend. Here, we present a method for objectively classifying the most informative regions of animal paths. We apply this method to flight trajectories from homing pigeons to identify probable locations of salient visual landmarks. We construct and apply a Gaussian process model of flight trajectory generation for pigeons trained to home from specific release sites. The model shows increasing predictive power as the birds become familiar with the sites, mirroring the animal's learning process. We subsequently find that the most informative elements of the flight trajectories coincide with landscape features that have previously been suggested as important components of the homing task.

Consequences of 'load-lightening' for future indirect fitness gains by helpers in a cooperatively breeding bird.

1. Helpers that invest energy in provisioning the offspring of related individuals stand to gain indirect fitness benefits from doing so. First, if the helper's effort is additional to that of the parents (additive) the productivity of the current breeding attempt can be increased. Secondly, if the parents reduce their workload (compensation) this can result in future indirect fitness gains to the helper via increased breeder survival; termed 'load-lightening'. 2. Long-tailed tits (Aegithalos caudatus) have a cooperative breeding system in which helpers assist kin and parents exhibit both additive and compensatory reactions in the presence of helpers. Offspring from helped nests are heavier and more likely to recruit into the breeding population, thus helpers gain indirect fitness benefits from increasing the productivity of the current breeding attempt. Despite breeders' reduction of feeding effort in the presence of helpers, previous investigations found no subsequent increase in breeder survival. 3. The aim of this study was to test the hypothesis that load-lightening resulted in indirect fitness benefits for helpers. We used data from a 14-year study to investigate the provisioning rate, survival and future fecundity of male and female long-tailed tits that did and did not receive help at the nest. 4. We found an asymmetrical response to the presence of helpers at large brood sizes. Males reduced their feeding rate more than females, and this differential response was reflected in a significant increase in male survival when provisioning large broods assisted by helpers. We found no evidence of any increase in future fecundity for helped breeders. 5. The finding that males reduce their provisioning rate in the presence of helpers (at large brood sizes) to a greater degree than females, and that this is reflected in an increase in survival rate for males only, implies that the survival increase is caused by the reduction in work-rate rather than a non-specific benefit of a larger group size. 6. The marginal benefits of help for breeder survival are likely to be more difficult to identify than the increased productivity at helped nests, but should not be overlooked when investigating the potential indirect fitness gains that supernumeraries can accrue by helping.

Flight dynamics of Cory's shearwater foraging in a coastal environment.

Flight dynamics theories are influenced by two major topics: how birds adapt their flight to cope with heterogeneous habitats, and whether birds plan to use the wind field or simply experience it. The aim of this study was to understand the flight dynamics of free-flying Cory's shearwaters in relation to the wind characteristics on the coastal upwelling region of continental Portugal. We deployed recently miniaturised devices-global positioning system loggers to collect precise and detailed information on birds' positions and motions. Prevalent winds were blowing from the north-east and adults used those winds by adjusting their flight directions mainly towards north-west and south-west, flying with cross and tail winds, respectively, and avoiding head winds. This is confirmation that Cory's shearwaters use a shear soaring flying strategy while exploiting the environment for food: adults foraged mainly with cross winds and their ground speed was not constant during all foraging trips as it changed dynamically as a result of the ocean surface shear winds. During travelling phases, ground speed was strongly influenced by the position of the bird with regard to the wind direction, as ground speed increased significantly with increasing tail wind component (TWC) values. Adults appear to choose foraging directions to exploit ambient wind, in order to improve shear soaring efficiency (cross winding) and exploit diurnal changes in tail wind strength to maximise commuting efficiency. We report, for the first time, precise ground speed values (GPS-derived data) and computed actual flight speed values (using TWC analysis) for Cory's shearwater.

Pigeons combine compass and landmark guidance in familiar route navigation.

How do birds orient over familiar terrain? In the best studied avian species, the homing pigeon (Columba livia), two apparently independent primary mechanisms are currently debated: either memorized visual landmarks provide homeward guidance directly, or birds rely on a compass to home from familiar locations. Using miniature Global Positioning System tracking technology and clock-shift procedures, we set sun-compass and landmark information in conflict, showing that experienced birds can accurately complete their memorized routes by using landmarks alone. Nevertheless, we also find that route following is often consistently offset in the expected compass direction, faithfully reproducing the shape of the track, but in parallel. Thus, we demonstrate conditions under which compass orientation and landmark guidance must be combined into a system of simultaneous or oscillating dual control.

From compromise to leadership in pigeon homing.

A central problem faced by animals traveling in groups is how navigational decisions by group members are integrated, especially when members cannot assess which individuals are best informed or have conflicting information or interests . Pigeons are now known to recapitulate faithfully their individually distinct habitual routes home , and this provides a novel paradigm for investigating collective decisions during flight under varying levels of interindividual conflict. Using high-precision GPS tracking of pairs of pigeons, we found that if conflict between two birds' directional preferences was small, individuals averaged their routes, whereas if conflict rose over a critical threshold, either the pair split or one of the birds became the leader. Modeling such paired decision-making showed that both outcomes-compromise and leadership-could emerge from the same set of simple behavioral rules. Pairs also navigated more efficiently than did the individuals of which they were composed, even though leadership was not necessarily assumed by the more efficient bird. In the context of mass migration of birds and other animals, our results imply that simple self-organizing rules can produce behaviors that improve accuracy in decision-making and thus benefit individuals traveling in groups .

An edge-detection approach to investigating pigeon navigation.

This study brings together work in pattern recognition and animal behaviour. By applying algorithms in pattern recognition, we examined how visual landscape information influences pigeons' homing behaviour. We used an automated procedure (Canny edge detector) to extract edges from an aerial image of the experimental terrain. Analysis of pigeons' homing routes recorded using global positioning system (GPS) trackers showed that the chosen homing paths, as well as changes in the birds' navigational states, tended to coincide with these edges. This study demonstrates that some edge-containing land features attract homing pigeons and trigger changes in their navigational states.

Homing pigeons develop local route stereotypy.

The mechanisms used by homing pigeons (Columba livia) to navigate homeward from distant sites have been well studied, yet the mechanisms underlying navigation within, and mapping of, the local familiar area have been largely neglected. In the local area pigeons pote ntially have access to a powerful navigational aid--a memorized landscape map. Current opinion suggests that landmarks are used only to recognize a familiar start position and that the goalward route is then achieved solely using compass orientation. We used high-resolution global positioning system (GPS) loggers to track homing pigeons as they became progressively familiar with a local homing task. Here, we demonstrate that birds develop highly stereotyped yet individually distinctive routes over the landscape, which remain substantially inefficient. Precise aerial route recapitulation implies close control by localized geocentric cues. Magnetic cues are unlikely to have been used, since recapitulation remains despite magnetic disruption treatment, and olfactory cues would have been positionally unstable under the variable wind conditions, making visual landmarks the most likely cues used.

Familiar route loyalty implies visual pilotage in the homing pigeon.

Wide-ranging animals, such as birds, regularly traverse large areas of the landscape efficiently in the course of their local movement patterns, which raises fundamental questions about the cognitive mechanisms involved. By using precision global-positioning-system loggers, we show that homing pigeons (Columba livia) not only come to rely on highly stereotyped yet surprisingly inefficient routes within the local area but are attracted directly back to their individually preferred routes even when released from novel sites off-route. This precise route loyalty demonstrates a reliance on familiar landmarks throughout the flight, which was unexpected under current models of avian navigation. We discuss how visual landmarks may be encoded as waypoints within familiar route maps.