A vision for incorporating human mobility in the study of human-wildlife interactions.

As human activities increasingly shape land- and seascapes, understanding human-wildlife interactions is imperative for preserving biodiversity. Habitats are impacted not only by static modifications, such as roads, buildings and other infrastructure, but also by the dynamic movement of people and their vehicles occurring over shorter time scales. Although there is increasing realization that both components of human activity substantially affect wildlife, capturing more dynamic processes in ecological studies has proved challenging. Here we propose a conceptual framework for developing a 'dynamic human footprint' that explicitly incorporates human mobility, providing a key link between anthropogenic stressors and ecological impacts across spatiotemporal scales. Specifically, the dynamic human footprint integrates a range of metrics to fully acknowledge the time-varying nature of human activities and to enable scale-appropriate assessments of their impacts on wildlife behaviour, demography and distributions. We review existing terrestrial and marine human-mobility data products and provide a roadmap for how these could be integrated and extended to enable more comprehensive analyses of human impacts on biodiversity in the Anthropocene.

Contrasting parental roles shape sex differences in poison frog space use but not navigational performance.

Sex differences in vertebrate spatial abilities are typically interpreted under the adaptive specialization hypothesis, which posits that male reproductive success is linked to larger home ranges and better navigational skills. The androgen spillover hypothesis counters that enhanced male spatial performance may be a byproduct of higher androgen levels. Animal groups that include species where females are expected to outperform males based on life-history traits are key for disentangling these hypotheses. We investigated the association between sex differences in reproductive strategies, spatial behavior, and androgen levels in three species of poison frogs. We tracked individuals in natural environments to show that contrasting parental sex roles shape sex differences in space use, where the sex performing parental duties shows wider-ranging movements. We then translocated frogs from their home areas to test their navigational performance and found that the caring sex outperformed the non-caring sex only in one out of three species. In addition, males across species displayed more explorative behavior than females and androgen levels correlated with explorative behavior and homing accuracy. Overall, we reveal that poison frog reproductive strategies shape movement patterns but not necessarily navigational performance. Together this work suggests that prevailing adaptive hypotheses provide an incomplete explanation of sex differences in spatial abilities.

The spatial and temporal exploitation of anthropogenic food sources by common ravens (Corvus corax) in the Alps.

BACKGROUND: Anthropogenic food sources (AFSs) are widespread in human-transformed landscapes and the current scale at which they occur drives ecological change at the individual, population, and community levels. AFSs are exploited extensively by common ravens, Corvus corax. Understanding how raven populations use AFSs can provide insight into their ecological responses to AFSs. METHODS: We equipped 81 ravens in the Austrian Alps with GPS-transmitters over a period of 2.75 years. Using these tracking data, we investigated how cohort differences (i.e., age, sex, and origin) and seasonal changes influence raven movement patterns (i.e., occurrence distribution and maximum daily displacement) and AFS-use (i.e., number of AFSs visited and probability of being present at any AFS) at 45 extensively exploited sites. RESULTS: We found that proxies for experience and dominance, inferred by age (i.e., juvenile versus adult) and origin (i.e., wild-caught versus captive-bred-released) cohorts, influenced movement patterns and the number of AFSs visited. However, all individuals were equally likely to be present at AFSs, highlighting the importance of AFSs for non-breeders in the study population. Seasonal changes in environmental conditions that affect energetic demands, the availability of natural and anthropogenic food, and foraging competition,  influenced individuals' occurrence distributions and AFS-use. We found that under harsher conditions in autumn and winter, individuals ranged wider and depended on AFSs to a larger degree. However, contrary to expectation, they were less likely to be present at AFSs in these seasons compared to spring and summer, suggesting a trade-off between time spent moving and exploiting resources. We attribute the small ranging movements exhibited by non-breeders in spring and summer to the presence of highly territorial and socially dominant breeders. As breeders mostly stay and forage within their territories during these seasons, competition at AFSs decrease, thereby increasing the likelihood of individuals being present at any AFS. CONCLUSIONS: We emphasize that movement and AFS-use differ according to cohort differences and the seasonality of the environment. Our results highlight that predictable AFSs affect foraging strategies among non-breeding ravens. The extent of AFS-exploitation among non-breeding ravens in our study emphasize the potential of AFSs in shaping raven movement and resource-use.

Tapping into non-English-language science for the conservation of global biodiversity.

The widely held assumption that any important scientific information would be available in English underlies the underuse of non-English-language science across disciplines. However, non-English-language science is expected to bring unique and valuable scientific information, especially in disciplines where the evidence is patchy, and for emergent issues where synthesising available evidence is an urgent challenge. Yet such contribution of non-English-language science to scientific communities and the application of science is rarely quantified. Here, we show that non-English-language studies provide crucial evidence for informing global biodiversity conservation. By screening 419,679 peer-reviewed papers in 16 languages, we identified 1,234 non-English-language studies providing evidence on the effectiveness of biodiversity conservation interventions, compared to 4,412 English-language studies identified with the same criteria. Relevant non-English-language studies are being published at an increasing rate in 6 out of the 12 languages where there were a sufficient number of relevant studies. Incorporating non-English-language studies can expand the geographical coverage (i.e., the number of 2° × 2° grid cells with relevant studies) of English-language evidence by 12% to 25%, especially in biodiverse regions, and taxonomic coverage (i.e., the number of species covered by the relevant studies) by 5% to 32%, although they do tend to be based on less robust study designs. Our results show that synthesising non-English-language studies is key to overcoming the widespread lack of local, context-dependent evidence and facilitating evidence-based conservation globally. We urge wider disciplines to rigorously reassess the untapped potential of non-English-language science in informing decisions to address other global challenges. Please see the Supporting information files for Alternative Language Abstracts.

Cooperation with closely bonded individuals reduces cortisol levels in long-tailed macaques.

Many animal species cooperate with conspecifics in various social contexts. While ultimate causes of cooperation are being studied extensively, its proximate causes, particularly endocrine mechanisms, have received comparatively little attention. Here, we present a study investigating the link between the hormone cortisol, cooperation and social bonds in long-tailed macaques (Macaca fascicularis). We tested 14 macaques in a dyadic cooperation task (loose-string paradigm), each with two partners of different social bond strength and measured their salivary cortisol before and after the task. We found no strong link between the macaques' cortisol level before the task and subsequent cooperative success. By contrast, we did find that the act of cooperating in itself led to a subsequent decrease in cortisol levels, but only when cooperating with closely bonded individuals. Two control conditions showed that this effect was not due to the mere presence of such an individual or the pulling task itself. Consequently, our study shows an intricate way in which the hypothalamic-pituitary-adrenal axis is involved in cooperation. Future studies should reveal whether and how our findings are driven by the anxiolytic effect of oxytocin, which has been associated with social bonding.

Experience shapes accuracy in territorial decision-making in a poison frog.

The trade-off between speed and accuracy affects many behavioural processes like predator avoidance, foraging and nest-site selection, but little is known about this trade-off relative to territorial behaviour. Some poison frogs are highly territorial and fiercely repel calling male intruders. However, attacks need to be conducted cautiously, as they are energetically costly and bear the risk of own injury or accidentally targeting the wrong individual. In this study, we investigated the speed-accuracy trade-off in the context of male territoriality during the breeding season in the brilliant-thighed poison frog, Allobates femoralis. In our experiment, we presented the call of an invisible 'threatening' intruder together with a visible 'non-threatening' intruder, using acoustic playback and a frog model, respectively. Contrary to our prediction, neither reaction time nor approach speed of the tested frogs determined the likelihood of erroneous attacks. However, younger individuals were more likely to attack the non-threatening model than older ones, suggesting that experience plays an essential role in identifying and distinguishing rivalling individuals in a territorial context.

Decision time modulates social foraging success in wild common ravens, Corvus corax.

Social foraging provides several benefits for individuals but also bears the potential costs of higher competition. In some species, such competition arises through kleptoparasitism, that is when an animal takes food which was caught or collected by a member of its social group. Except in the context of caching, few studies have investigated how individuals avoid kleptoparasitism, which could be based on physical strength/dominance but also cognitive skills. Here, we investigated the foraging success of wild common ravens, Corvus corax, experiencing high levels of kleptoparasitism from conspecifics when snatching food from the daily feedings of captive wild boars in a game park in the Austrian Alps. Success in keeping the food depended mainly on the individuals' age class and was positively correlated with the time to make a decision in whether to fly off with food or consume it on site. While the effect of age class suggests that dominant and/or experienced individuals are better in avoiding kleptoparasitism, the effect of decision time indicates that individuals benefit from applying cognition to such decision-making, independently of age class. We discuss our findings in the context of the ecological and social intelligence hypotheses referring to the development of cognitive abilities. We conclude that investigating which factors underline kleptoparasitism avoidance is a promising scenario to test specific predictions derived from these hypotheses.

How far do tadpoles travel in the rainforest? Parent-assisted dispersal in poison frogs.

Parents can influence offspring dispersal through breeding site selection, competition, or by directly moving their offspring during parental care. Many animals move their young, but the potential role of this behavior in dispersal has rarely been investigated. Neotropical poison frogs (Dendrobatidae) are well known for shuttling their tadpoles from land to water, but the associated movements have rarely been quantified and the potential function of tadpole transport in dispersal has not been addressed. We used miniature radio-transmitters to track the movements of two poison frog species during tadpole transport, and surveyed pool availability in the study area. We found that parental males move farther than expected by the distance to the nearest pool and spread their offspring across multiple pools. We argue that these movement patterns cannot be fully explained by pool quality and availability, and suggest that adaptive benefits related to offspring dispersal also shape the spatial behavior of parental frogs.

What constitutes "social complexity" and "social intelligence" in birds? Lessons from ravens.

In the last decades, the assumption that complex social life is cognitively challenging, and thus can drive mental evolution, has received much support from empirical studies in nonhuman primates. While extending the scope to other mammals and birds, different views have been adopted on what constitutes social complexity and which specific cognitive skills are selected for. Notably, many avian species form "open" groups as non-breeders (i.e., seasonally and before sexual maturity) that have been largely ignored as potential sources of social complexity. Reviewing 30 years of research on ravens, we illustrate the socio-ecological conditions faced by these birds as non-breeders and discuss how these relate to their socio-cognitive skills. We argue that the non-breeding period is key to understand raven social life and, to a larger extent, avian social life in general. We furthermore emphasize how the combination of the large-scale perspective (defining social system components: e.g., social organization, mating system) and the individual-scale perspective on social systems allows to better capture the complete set of social challenges experienced by individuals throughout their life, ultimately resulting on a more comprehensive understanding of species' social complexity.

Seasonal differences of corticosterone metabolite concentrations and parasite burden in northern bald ibis (Geronticus eremita): The role of affiliative interactions.

The reproductive season is energetically costly as revealed by elevated glucocorticoid concentrations, constrained immune functions and an increased risk of infections. Social allies and affiliative interactions may buffer physiological stress responses and thereby alleviate associated effects. In the present study, we investigated the seasonal differences of immune reactive corticosterone metabolite concentrations, endoparasite burden (nematode eggs and coccidian oocysts) and affiliative interactions in northern bald ibis (Geronticus eremita), a critically endangered bird. In total, 43 individually marked focal animals from a free-ranging colony were investigated. The analyses included a description of initiated and received affiliative interactions, pair bond status as well as seasonal patterns of hormone and endoparasite levels. During the reproductive season, droppings contained parasite eggs more often and corticosterone metabolite levels were higher as compared to the period after reproduction. The excretion rate of endoparasite products was lower in paired individuals than in unpaired ones, but paired animals exhibited higher corticosterone metabolite concentrations than unpaired individuals. Furthermore, paired individuals initiated affiliative behaviour more frequently than unpaired ones. This suggests that the reproductive season influences the excretion patterns of endoparasite products and corticosterone metabolites and that affiliative interactions between pair partners may positively affect endoparasite burden during periods of elevated glucocorticoid levels. Being embedded in a pair bond may have a positive impact on individual immune system and parasite resistance.

Map-like navigation from distances exceeding routine movements in the three-striped poison frog (Ameerega trivittata).

Most animals move in dense habitats where distant landmarks are limited, but how they find their way around remains poorly understood. Poison frogs inhabit the rainforest understory, where they shuttle tadpoles from small territories to widespread pools. Recent studies revealed their excellent spatial memory and the ability to home back from several hundred meters. It remains unclear whether this homing ability is restricted to the areas that had been previously explored or whether it allows the frogs to navigate from areas outside their direct experience. Here, we used radio-tracking to study the navigational performance of three-striped poison frog translocated outside the area of their routine movements (200-800 m). Translocated frogs returned to their home territory via a direct path from all distances and with little difference in orientation accuracy, suggesting a flexible map-like navigation mechanism. These findings challenge our current understanding of both the mechanisms and the sensory basis of amphibian orientation.

Relying on known or exploring for new? Movement patterns and reproductive resource use in a tadpole-transporting frog.

Animals relying on uncertain, ephemeral and patchy resources have to regularly update their information about profitable sites. For many tropical amphibians, widespread, scattered breeding pools constitute such fluctuating resources. Among tropical amphibians, poison frogs (Dendrobatidae) exhibit some of the most complex spatial and parental behaviors-including territoriality and tadpole transport from terrestrial clutches to ephemeral aquatic deposition sites. Recent studies have revealed that poison frogs rely on spatial memory to successfully navigate through their environment. This raises the question of when and how these frogs gain information about the area and suitable reproductive resources. To investigate the spatial patterns of pool use and to reveal potential explorative behavior, we used telemetry to follow males of the territorial dendrobatid frog Allobates femoralis during tadpole transport and subsequent homing. To elicit exploration, we reduced resource availability experimentally by simulating desiccated deposition sites. We found that tadpole transport is strongly directed towards known deposition sites and that frogs take similar direct paths when returning to their home territory. Frogs move faster during tadpole transport than when homing after the deposition, which probably reflects different risks and costs during these two movement phases. We found no evidence for exploration, neither during transport nor homing, and independent of the availability of deposition sites. We suggest that prospecting during tadpole transport is too risky for the transported offspring as well as for the transporting male. Relying on spatial memory of multiple previously discovered pools appears to be the predominant and successful strategy for the exploitation of reproductive resources in A. femoralis. Our study provides for the first time a detailed description of poison frog movement patterns during tadpole transport and corroborates recent findings on the significance of spatial memory in poison frogs. When these frogs explore and discover new reproductive resources remains unknown.

Fission-fusion dynamics over large distances in raven non-breeders.

The influence of fission-fusion dynamics, i.e., temporal variation in group size and composition, on social complexity has been studied in large-brained mammals that rely on social bonds. Little is known about birds, even though some species like ravens have recently received attention for their socio-cognitive skills and use of social bonds. While raven breeders defend territories year-round, non-breeders roam through large areas and form groups at food sources or night roosts. We here examined the fission-fusion patterns of non-breeding ravens over years, investigating whether birds meet repeatedly either at the same or at different locations. We combined four large datasets: presence-absence observations from two study sites (Austria, Italy) and GPS-tracking of ravens across two study areas (Austria, France). As expected, we found a highly dynamic system in which individuals with long phases of temporary settlement had a high probability of meeting others. Although GPS-tagged ravens spread out over thousands of square kilometres, we found repeated associations between almost half of the possible combinations at different locations. Such a system makes repeated interactions between individuals at different sites possible and likely. High fission-fusion dynamics may thus not hinder but shape the social complexity of ravens and, possibly, other long-term bonded birds.

GPS tracking of non-breeding ravens reveals the importance of anthropogenic food sources during their dispersal in the Eastern Alps.

In many songbirds, the space use of breeders is well studied but poorly understood for non-breeders. In common ravens, some studies of non-breeders indicate high vagrancy with large individual differences in home range size, whereas others show that up to 40% of marked non-breeders can be regularly observed at the same anthropogenic food source over months to years. The aim of this study was to provide new insights on ravens' behavior during dispersal in the Eastern Alps. We deployed Global Positioning System (GPS) loggers on 10 individuals to gather accurate spatial and temporal information on their movements to quantify: 1) the dimension of the birds' space use (home range size with seasonal effects and daily/long-term travel distances), 2) how long they stayed in a dispersal stage of wandering as opposed to settling temporarily, and 3) their destination of movements. We recorded movements of up to 40 km per hour, more than 160 km within 1 day and more than 11,000 km within 20 months, indicating high vagrancy. Switching frequently between temporarily settling and travelling large distances in short time intervals leads to extensive home ranges, which also explains and combines the different findings in the literature. The destinations are rich anthropogenic food sources, where the birds spent on average 75% of their time. We discuss how ravens may find these "feeding hot spots" and which factors may influence their decision to stay/leave a site. The strong dependence on anthropogenic resources found in this population may have implications for site management and conservation issues.

Homing trajectories and initial orientation in a Neotropical territorial frog, Allobates femoralis (Dendrobatidae).

INTRODUCTION: The ability to relocate home or breeding sites after experimental removal has been observed in several amphibians and the sensory basis of this behavior has been studied in some temperate-region species. However, the actual return trajectories have rarely been quantified in these studies and it remains unknown how different cues guide the homing behavior. Dendrobatidae (dart-poison frogs) exhibit some of the most complex spatial behaviors among amphibians, such as territoriality and tadpole transport. Recent data showed that Allobates femoralis, a frog with paternal tadpole transport, successfully returns to the home territories after experimental translocations of up to 400 m. In the present study, we used harmonic direction finding to obtain homing trajectories. Additionally, we quantified the initial orientation of individuals, translocated 10 m to 105 m, in an arena assay. RESULTS: Tracking experiments revealed that homing trajectories are characterized by long periods of immobility (up to several days) and short periods (several hours) of rapid movement, closely fitting a straight line towards the home territory. In the arena assay, the frogs showed significant homeward orientation for translocation distances of 35 m to 70 m but not for longer and shorter distances. CONCLUSIONS: Our results describe a very accurate homing behavior in male A. femoralis. The straightness of trajectories and initial homeward orientation suggest integration of learned landmarks providing a map position for translocated individuals. Future research should focus on the role of learning in homing behavior and the exact nature of cues being used.

Don't get the blues: conspicuous nuptial colouration of male moor frogs (Rana arvalis) supports visual mate recognition during scramble competition in large breeding aggregations.

Conspicuous male colouration is expected to have evolved primarily through selection by female choice. In what way conspicuous colours could be advantageous to males scrambling for mates remains largely unknown. The moor frog (Rana arvalis) belongs to the so-called explosive breeders in which spawning period is short; intrasexual competition is strong, and males actively search and scramble for females. During breeding, male body colouration changes from a dull brown (similar to females) to a conspicuous blue, and we wanted to test if male blueness influences mating success or facilitates male mate recognition. To do so, we first measured the colour of mated and non-mated males using a spectrophotometer. In an experiment, we then analysed interactions of actual male moor frogs in natural spawning aggregations with a brown (resembling a female or a non-breeding male) and a blue model frog. Mated and non-mated males did not differ in colouration, suggesting that female choice based on colour traits was unlikely. In our behavioural experiment, male moor frogs spent significantly more time in contact and in amplexus with the brown model than with the blue model. Our results suggest that the nuptial colouration in moor frogs can act as a new type of visual signal in anurans evolved to promote instantaneous mate recognition allowing males to quickly move between rivals while scrambling for females. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1007/s00265-012-1412-6) contains supplementary material, which is available to authorized users.

Ontogeny of Social Relations and Coalition Formation in Common Ravens (Corvus corax).

The social intelligence hypothesis, originally developed for primates to explain their high intelligence and large relative brain size, assumes that challenges posed by social life in complex societies with many group members lead to the evolution of advanced cognitive abilities. In birds, pair-bonded species have larger brains than non-pair bonded species, indicating that the quality of social relationships better predicts social complexity than group size. Ravens are a long-term monogamous and territorial species, renowned for their sophisticated socio-cognitive skills and complex social relationships. Notably, during their early years they live in fission-fusion-like non-breeder societies in which social relationships could be of particular importance. Here we observed the development of dominance and affiliative relationships in 12 hand-raised captive ravens, examining the influence of age, sex and kinship on social interactions. Furthermore, we investigated at which developmental step a stable hierarchy emerged, whether third-party interventions played a role and how selectively birds intervened in others' conflicts. At 4-5 months post-fledging, we found an increase in socio-positive behaviour and a decrease in aggression, along with the establishment of a linear dominance rank hierarchy. In line with kin selection theory, siblings exhibited a greater degree of tolerance and engaged in more socio-positive behaviour. In their first few months, ravens frequently intervened in others' conflicts but supported mainly the aggressor; later on, their support became more selective towards kin and close social partners. These findings indicate that ravens engage in sophisticated social behaviours and form stable relationships already in their first year of life.

Northern bald ibises follow others' gaze into distant space but not behind barriers.

Gaze following is the ability to use the visual orientation of others as a trigger to look in the same direction. Thereby, animals may either align their head and eye orientation with others (gaze following into distant space) or may even reposition themselves to look behind barriers impairing their perception (geometrical gaze following). It has been proposed that these two different modes are functionally and cognitively distinct, but experimental evidence for this claim is lacking. We here, to our knowledge, demonstrate for the first time, that adult animals may be capable of following gaze into distant space, but not geometrically around barriers. We tested Northern bald ibises (Geronticus eremita) for their ability to follow a conspecific's gaze in two standard tasks. The birds readily looked up after seeing a model bird looking up; however, when seeing a model looking behind a barrier, they responded by looking at the barrier instead of walking around. These findings are in stark contrast to results obtained with great apes and corvids and provide the first experimental evidence, to our knowledge, for cognitive differences in gaze following tasks.

Novel object exploration in ravens (Corvus corax): effects of social relationships.

Social context has been shown to encourage, or to delay object exploration and learning. This ambiguity might be due to factors such as social relationships and personality of the individuals involved. Here, we investigated in ravens (Corvus corax) individuals' consistency in response to novel objects over development and across contexts: alone versus social. In the social setting we focussed on the effects of social relationships on social facilitation during the approach to novel objects. We tested 11 hand-raised ravens with novel objects individually at three and six months of age and in dyadic combinations at six months of age. Individuals were consistent over development and contexts in their response to different novel objects. Birds joined siblings faster to approach novel objects than non-siblings. They also spent more time sitting close to siblings than to non-siblings. In male-male dyads but not in female-female dyads, subordinates approached the novel objects significantly faster than dominant birds. In contrast, dominant males were the first to approach the novel objects in mixed-sex combinations. Hence, the effect of social context seems to depend on the social relationships towards the companions and on the combination of the sexes.