Publications by authors named "Ran Nathan"

52 Publications

Spatial cognitive ability is associated with transitory movement speed but not straightness during the early stages of exploration.

R Soc Open Sci 2021 Mar 10;8(3):201758. Epub 2021 Mar 10.

Centre for Research in Animal Behaviour, Psychology, University of Exeter, Exeter EX4 4QG, UK.

Memories about the spatial environment, such as the locations of foraging patches, are expected to affect how individuals move around the landscape. However, individuals differ in the ability to remember spatial locations (spatial cognitive ability) and evidence is growing that these inter-individual differences influence a range of fitness proxies. Yet empirical evaluations directly linking inter-individual variation in spatial cognitive ability and the development and structure of movement paths are lacking. We assessed the performance of young pheasants () on a spatial cognition task before releasing them into a novel, rural landscape and tracking their movements. We quantified changes in the straightness and speed of their transitory paths over one month. Birds with better performances on the task initially made slower transitory paths than poor performers but by the end of the month, there was no difference in speed. In general, birds increased the straightness of their path over time, indicating improved efficiency independent of speed, but this was not related to performance on the cognitive task. We suggest that initial slow movements may facilitate more detailed information gathering by better performers and indicates a potential link between an individual's spatial cognitive ability and their movement behaviour.
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http://dx.doi.org/10.1098/rsos.201758DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8074888PMC
March 2021

An evaluation of machine learning classifiers for next-generation, continuous-ethogram smart trackers.

Mov Ecol 2021 Mar 30;9(1):15. Epub 2021 Mar 30.

Centre for Integrative Ecology, School of Life and Environmental Sciences, Deakin University, Geelong, Victoria, Australia.

Background: Our understanding of movement patterns and behaviours of wildlife has advanced greatly through the use of improved tracking technologies, including application of accelerometry (ACC) across a wide range of taxa. However, most ACC studies either use intermittent sampling that hinders continuity or continuous data logging relying on tracker retrieval for data downloading which is not applicable for long term study. To allow long-term, fine-scale behavioural research, we evaluated a range of machine learning methods for their suitability for continuous on-board classification of ACC data into behaviour categories prior to data transmission.

Methods: We tested six supervised machine learning methods, including linear discriminant analysis (LDA), decision tree (DT), support vector machine (SVM), artificial neural network (ANN), random forest (RF) and extreme gradient boosting (XGBoost) to classify behaviour using ACC data from three bird species (white stork Ciconia ciconia, griffon vulture Gyps fulvus and common crane Grus grus) and two mammals (dairy cow Bos taurus and roe deer Capreolus capreolus).

Results: Using a range of quality criteria, SVM, ANN, RF and XGBoost performed well in determining behaviour from ACC data and their good performance appeared little affected when greatly reducing the number of input features for model training. On-board runtime and storage-requirement tests showed that notably ANN, RF and XGBoost would make suitable on-board classifiers.

Conclusions: Our identification of using feature reduction in combination with ANN, RF and XGBoost as suitable methods for on-board behavioural classification of continuous ACC data has considerable potential to benefit movement ecology and behavioural research, wildlife conservation and livestock husbandry.
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http://dx.doi.org/10.1186/s40462-021-00245-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8011142PMC
March 2021

Is habitat selection in the wild shaped by individual-level cognitive biases in orientation strategy?

Ecol Lett 2021 Apr 22;24(4):751-760. Epub 2021 Feb 22.

Centre for Research in Animal Behaviour, Psychology, University of Exeter, Exeter, EX4 4QG, UK.

Cognitive biases for encoding spatial information (orientation strategies) in relation to self (egocentric) or landmarks (allocentric) differ between species or populations according to the habitats they occupy. Whether biases in orientation strategy determine early habitat selection or if individuals adapt their biases following experience is unknown. We determined orientation strategies of pheasants, Phasianus colchicus, using a dual-strategy maze with an allocentric probe trial, before releasing them (n = 20) into a novel landscape, where we monitored their movement and habitat selection. In general, pheasants selected for woodland over non-woodland habitat, but allocentric-biased individuals exhibited weaker avoidance of non-woodland habitat, where we expected allocentric navigation to be more effective. Sex did not influence selection but was associated with speed and directional persistence in non-woodland habitat. Our results suggest that an individual's habitat selection is associated with inherent cognitive bias in early life, but it is not yet clear what advantages this may offer.
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http://dx.doi.org/10.1111/ele.13694DOI Listing
April 2021

Early-life behaviour predicts first-year survival in a long-distance avian migrant.

Proc Biol Sci 2021 01 13;288(1942):20202670. Epub 2021 Jan 13.

Movement Ecology Laboratory, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel.

Early-life conditions have critical, long-lasting effects on the fate of individuals, yet early-life activity has rarely been linked to subsequent survival of animals in the wild. Using high-resolution GPS and body-acceleration data of 93 juvenile white storks (), we examined the links between behaviour during both pre-fledging and post-fledging (fledging-to-migration) periods and subsequent first-year survival. Juvenile daily activity (based on overall dynamic body acceleration) showed repeatable between-individual variation, the juveniles' pre- and post-fledging activity levels were correlated and both were positively associated with subsequent survival. Daily activity increased gradually throughout the post-fledging period, and the relationship between post-fledging activity and survival was stronger in individuals who increased their daily activity level faster (an interaction effect). We suggest that high activity profiles signified individuals with increased pre-migratory experience, higher individual quality and perhaps more proactive personality, which could underlie their superior survival rates. The duration of individuals' fledging-to-migration periods had a hump-shaped relationship with survival: higher survival was associated with intermediate rather than short or long durations. Short durations reflect lower pre-migratory experience, whereas very long ones were associated with slower increases in daily activity level which possibly reflects slow behavioural development. In accordance with previous studies, heavier nestlings and those that hatched and migrated earlier had increased survival. Using extensive tracking data, our study exposed new links between early-life attributes and survival, suggesting that early activity profiles in migrating birds can explain variation in first-year survival.
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http://dx.doi.org/10.1098/rspb.2020.2670DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7892428PMC
January 2021

Migration, pathogens and the avian microbiome: A comparative study in sympatric migrants and residents.

Mol Ecol 2020 12 19;29(23):4706-4720. Epub 2020 Oct 19.

Movement Ecology Laboratory, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel.

Animals generally benefit from their gastrointestinal microbiome, but the factors that influence the composition and dynamics of their microbiota remain poorly understood. Studies of nonmodel host species can illuminate how microbiota and their hosts interact in natural environments. We investigated the role of migratory behaviour in shaping the gut microbiota of free-ranging barn swallows (Hirundo rustica) by studying co-occurring migrant and resident subspecies sampled during the autumn migration at a migratory bottleneck. We found that within-host microbial richness (α-diversity) was similar between migrant and resident microbial communities. In contrast, we found that microbial communities (β-diversity) were significantly different between groups regarding both microbes present and their relative abundances. Compositional differences were found for 36 bacterial genera, with 27 exhibiting greater abundance in migrants and nine exhibiting greater abundance in residents. There was heightened abundance of Mycoplasma spp. and Corynebacterium spp. in migrants, a pattern shared by other studies of migratory species. Screens for key regional pathogens revealed that neither residents nor migrants carried avian influenza viruses and Newcastle disease virus, suggesting that the status of these diseases did not underlie observed differences in microbiome composition. Furthermore, the prevalence and abundance of Salmonella spp., as determined from microbiome data and cultural assays, were both low and similar across the groups. Overall, our results indicate that microbial composition differs between migratory and resident barn swallows, even when they are conspecific and sympatrically occurring. Differences in host origins (breeding sites) may result in microbial community divergence, and varied behaviours throughout the annual cycle (e.g., migration) could further differentiate compositional structure as it relates to functional needs.
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http://dx.doi.org/10.1111/mec.15660DOI Listing
December 2020

Seasonal niche tracking of climate emerges at the population level in a migratory bird.

Proc Biol Sci 2020 09 23;287(1935):20201799. Epub 2020 Sep 23.

Institute for Biochemistry and Biology, University of Potsdam, D-14469, Potsdam, Germany.

Seasonal animal migration is a widespread phenomenon. At the species level, it has been shown that many migratory animal species track similar climatic conditions throughout the year. However, it remains unclear whether such a niche tracking pattern is a direct consequence of individual behaviour or emerges at the population or species level through behavioural variability. Here, we estimated seasonal niche overlap and seasonal niche tracking at the individual and population level of central European white storks (). We quantified niche tracking for both weather and climate conditions to control for the different spatio-temporal scales over which ecological processes may operate. Our results indicate that niche tracking is a bottom-up process. Individuals mainly track weather conditions while climatic niche tracking mainly emerges at the population level. This result may be partially explained by a high degree of intra- and inter-individual variation in niche overlap between seasons. Understanding how migratory individuals, populations and species respond to seasonal environments is key for anticipating the impacts of global environmental changes.
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http://dx.doi.org/10.1098/rspb.2020.1799DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7542805PMC
September 2020

Cognitive map-based navigation in wild bats revealed by a new high-throughput tracking system.

Science 2020 07;369(6500):188-193

Movement Ecology Lab, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, Faculty of Science, The Hebrew University of Jerusalem, Israel.

Seven decades of research on the "cognitive map," the allocentric representation of space, have yielded key neurobiological insights, yet field evidence from free-ranging wild animals is still lacking. Using a system capable of tracking dozens of animals simultaneously at high accuracy and resolution, we assembled a large dataset of 172 foraging Egyptian fruit bats comprising >18 million localizations collected over 3449 bat-nights across 4 years. Detailed track analysis, combined with translocation experiments and exhaustive mapping of fruit trees, revealed that wild bats seldom exhibit random search but instead repeatedly forage in goal-directed, long, and straight flights that include frequent shortcuts. Alternative, non-map-based strategies were ruled out by simulations, time-lag embedding, and other trajectory analyses. Our results are consistent with expectations from cognitive map-like navigation and support previous neurobiological evidence from captive bats.
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http://dx.doi.org/10.1126/science.aax6904DOI Listing
July 2020

Movement-mediated community assembly and coexistence.

Biol Rev Camb Philos Soc 2020 08 20;95(4):1073-1096. Epub 2020 Apr 20.

Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Altensteinstr. 34, 14195, Berlin, Germany.

Organismal movement is ubiquitous and facilitates important ecological mechanisms that drive community and metacommunity composition and hence biodiversity. In most existing ecological theories and models in biodiversity research, movement is represented simplistically, ignoring the behavioural basis of movement and consequently the variation in behaviour at species and individual levels. However, as human endeavours modify climate and land use, the behavioural processes of organisms in response to these changes, including movement, become critical to understanding the resulting biodiversity loss. Here, we draw together research from different subdisciplines in ecology to understand the impact of individual-level movement processes on community-level patterns in species composition and coexistence. We join the movement ecology framework with the key concepts from metacommunity theory, community assembly and modern coexistence theory using the idea of micro-macro links, where various aspects of emergent movement behaviour scale up to local and regional patterns in species mobility and mobile-link-generated patterns in abiotic and biotic environmental conditions. These in turn influence both individual movement and, at ecological timescales, mechanisms such as dispersal limitation, environmental filtering, and niche partitioning. We conclude by highlighting challenges to and promising future avenues for data generation, data analysis and complementary modelling approaches and provide a brief outlook on how a new behaviour-based view on movement becomes important in understanding the responses of communities under ongoing environmental change.
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http://dx.doi.org/10.1111/brv.12600DOI Listing
August 2020

Movement ecology and sex are linked to barn owl microbial community composition.

Mol Ecol 2020 04 7;29(7):1358-1371. Epub 2020 Apr 7.

Museum of Vertebrate Zoology, University of California, Berkeley, Berkeley, CA, USA.

The behavioural ecology of host species is likely to affect their microbial communities, because host sex, diet, physiology, and movement behaviour could all potentially influence their microbiota. We studied a wild population of barn owls (Tyto alba) and collected data on their microbiota, movement, diet, size, coloration, and reproduction. The composition of bacterial species differed by the sex of the host and female owls had more diverse bacterial communities than their male counterparts. The abundance of two families of bacteria, Actinomycetaceae and Lactobacillaceae, also varied between the sexes, potentially as a result of sex differences in hormones and immunological function, as has previously been found with Lactobacillaceae in the microbiota of mice. Male and female owls did not differ in the prey they brought to the nest, which suggests that dietary differences are unlikely to underlie the differences in their microbiota. The movement behaviour of the owls was associated with the host microbiota in both males and females because owls that moved further from their nest each day had more diverse bacterial communities than owls that stayed closer to their nests. This novel result suggests that the movement ecology of hosts can impact their microbiota, potentially on the basis of their differential encounters with new bacterial species as the hosts move and forage across the landscape. Overall, we found that many aspects of the microbial community are correlated with the behavioural ecology of the host and that data on the microbiota can aid in generating new hypotheses about host behaviour.
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http://dx.doi.org/10.1111/mec.15398DOI Listing
April 2020

Managing uncertainty in movement knowledge for environmental decisions.

Conserv Lett 2019 May-Jun;12(3):e12620. Epub 2018 Dec 3.

School of Natural Sciences, Zoology, Trinity College Dublin The University of Dublin Dublin 2 Ireland.

Species' movements affect their response to environmental change but movement knowledge is often highly uncertain. We now have well-established methods to integrate movement knowledge into conservation practice but still lack a framework to deal with uncertainty in movement knowledge for environmental decisions. We provide a framework that distinguishes two dimensions of species' movement that are heavily influenced by uncertainty: about movement and of movement to environmental decisions. Management decisions can be informed by their position in this knowledge-relevance space. We then outline a framework to support decisions around (1) increasing understanding of the relevance of movement knowledge, (2) increasing robustness of decisions to uncertainties and (3) improving knowledge on species' movement. Our decision-support framework provides guidance for managing movement-related uncertainty in systematic conservation planning, agri-environment schemes, habitat restoration and international biodiversity policy. It caters to different resource levels (time and funding) so that species' movement knowledge can be more effectively integrated into environmental decisions.
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http://dx.doi.org/10.1111/conl.12620DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6686712PMC
December 2018

Author Correction: Stochastic simulations reveal few green wave surfing populations among spring migrating herbivorous waterfowl.

Nat Commun 2019 Jul 22;10(1):3191. Epub 2019 Jul 22.

Movement Ecology Laboratory, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, 91904, Jerusalem, Israel.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41467-019-11151-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6646335PMC
July 2019

Insights and approaches using deep learning to classify wildlife.

Sci Rep 2019 05 31;9(1):8137. Epub 2019 May 31.

Dept. Env. Sci., Pol. & Manag., UC Berkeley, Berkeley, CA, United States.

The implementation of intelligent software to identify and classify objects and individuals in visual fields is a technology of growing importance to operatives in many fields, including wildlife conservation and management. To non-experts, the methods can be abstruse and the results mystifying. Here, in the context of applying cutting edge methods to classify wildlife species from camera-trap data, we shed light on the methods themselves and types of features these methods extract to make efficient identifications and reliable classifications. The current state of the art is to employ convolutional neural networks (CNN) encoded within deep-learning algorithms. We outline these methods and present results obtained in training a CNN to classify 20 African wildlife species with an overall accuracy of 87.5% from a dataset containing 111,467 images. We demonstrate the application of a gradient-weighted class-activation-mapping (Grad-CAM) procedure to extract the most salient pixels in the final convolution layer. We show that these pixels highlight features in particular images that in some cases are similar to those used to train humans to identify these species. Further, we used mutual information methods to identify the neurons in the final convolution layer that consistently respond most strongly across a set of images of one particular species. We then interpret the features in the image where the strongest responses occur, and present dataset biases that were revealed by these extracted features. We also used hierarchical clustering of feature vectors (i.e., the state of the final fully-connected layer in the CNN) associated with each image to produce a visual similarity dendrogram of identified species. Finally, we evaluated the relative unfamiliarity of images that were not part of the training set when these images were one of the 20 species "known" to our CNN in contrast to images of the species that were "unknown" to our CNN.
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http://dx.doi.org/10.1038/s41598-019-44565-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6544615PMC
May 2019

Stochastic simulations reveal few green wave surfing populations among spring migrating herbivorous waterfowl.

Nat Commun 2019 05 16;10(1):2187. Epub 2019 May 16.

Movement Ecology Laboratory, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, 91904, Jerusalem, Israel.

Tracking seasonally changing resources is regarded as a widespread proximate mechanism underpinning animal migration. Migrating herbivores, for example, are hypothesized to track seasonal foliage dynamics over large spatial scales. Previous investigations of this green wave hypothesis involved few species and limited geographical extent, and used conventional correlation that cannot disentangle alternative correlated effects. Here, we introduce stochastic simulations to test this hypothesis using 222 individual spring migration episodes of 14 populations of ten species of geese, swans and dabbling ducks throughout Europe, East Asia, and North America. We find that the green wave cannot be considered a ubiquitous driver of herbivorous waterfowl spring migration, as it explains observed migration patterns of only a few grazing populations in specific regions. We suggest that ecological barriers and particularly human disturbance likely constrain the capacity of herbivorous waterfowl to track the green wave in some regions, highlighting key challenges in conserving migratory birds.
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http://dx.doi.org/10.1038/s41467-019-09971-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6522631PMC
May 2019

Early arrival at breeding grounds: Causes, costs and a trade-off with overwintering latitude.

J Anim Ecol 2018 11 3;87(6):1627-1638. Epub 2018 Oct 3.

Movement Ecology Laboratory, Department of Ecology, Evolution and Behaviour, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel.

Early arrival at breeding grounds is of prime importance for migrating birds as it is known to enhance breeding success. Adults, males and higher quality individuals typically arrive earlier, and across years, early arrival has been linked to warmer spring temperatures. However, the mechanisms and potential costs of early arrival are not well understood. To deepen the understanding of arrival date differences between individuals and years, we studied them in light of the preceding spring migration behaviour and atmospheric conditions en route. GPS and body acceleration (ACC) data were obtained for 35 adult white storks (Ciconia ciconia) over five years (2012-2016). ACC records were translated to energy expenditure estimates (overall dynamic body acceleration; ODBA) and to behavioural modes, and GPS fixes were coupled with environmental parameters. At the interindividual level (within years), early arrival was attributed primarily to departing earlier for migration and from more northern wintering sites (closer to breeding grounds), rather than to migration speed. In fact, early-departing birds flew slower, experienced weaker thermal uplifts and expended more energy during flight, but still arrived earlier, emphasizing the cost and the significance of early departure. Individuals that wintered further south arrived later at the breeding grounds but did not produce fewer fledglings, presumably due to positive carry-over effects of advantageous wintering conditions (increased precipitation, vegetation productivity and daylight time). Therefore, early arrival increased breeding success only after controlling for wintering latitude. Males arrived slightly ahead of females. Between years, late arrival was linked to colder temperatures en route through two different mechanisms: stronger headwinds causing slower migration and lower thermal uplifts resulting in longer stopovers. This study showed that distinct migratory properties underlie arrival time variation within and between years. It highlighted (a) an overlooked cost of early arrival induced by unfavourable atmospheric conditions during migration, (b) an important fitness trade-off in storks between arrival date and wintering habitat quality and (c) mechanistic explanations for the negative temperature-arrival date correlation in soaring birds. Such understanding of arrival time can facilitate forecasting migrating species responses to climate changes.
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http://dx.doi.org/10.1111/1365-2656.12898DOI Listing
November 2018

Using accelerometry to compare costs of extended migration in an arctic herbivore.

Curr Zool 2017 Dec 3;63(6):667-674. Epub 2017 Oct 3.

Department of Bioscience, Aarhus University, Kalø, Grenåvej 14, Rønde DK-8410, Denmark.

Understanding how individuals manage costs during the migration period is challenging because individuals are difficult to follow between sites; the advent of hybrid Global Positioning System-acceleration (ACC) tracking devices enables researchers to link spatial and temporal attributes of avian migration with behavior for the first time ever. We fitted these devices on male Greenland white-fronted geese wintering at 2 sites (Loch Ken, Scotland and Wexford, Ireland) to understand whether birds migrating further during spring fed more on wintering and staging areas in advance of migration episodes. Although Irish birds flew significantly further (ca. 300 km) than Scottish birds during spring, their cumulative hours of migratory flight, flight speed during migration, and overall dynamic body ACC (i.e., a proxy for energy expenditure) were not significantly different. Further, Irish birds did not feed significantly more or expend significantly more energy in advance of migration episodes. These results suggest broad individual plasticity in this species, although Scottish birds arriving on breeding areas in Greenland with greater energy stores (because they migrated less) may be better prepared for food scarcity, which might increase their reproductive success.
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http://dx.doi.org/10.1093/cz/zox056DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5804222PMC
December 2017

Moving in the Anthropocene: Global reductions in terrestrial mammalian movements.

Science 2018 Jan;359(6374):466-469

U.S. Geological Survey, Massachusetts Cooperative Fish and Wildlife Research Unit, University of Massachusetts, Amherst, MA 01003, USA.

Animal movement is fundamental for ecosystem functioning and species survival, yet the effects of the anthropogenic footprint on animal movements have not been estimated across species. Using a unique GPS-tracking database of 803 individuals across 57 species, we found that movements of mammals in areas with a comparatively high human footprint were on average one-half to one-third the extent of their movements in areas with a low human footprint. We attribute this reduction to behavioral changes of individual animals and to the exclusion of species with long-range movements from areas with higher human impact. Global loss of vagility alters a key ecological trait of animals that affects not only population persistence but also ecosystem processes such as predator-prey interactions, nutrient cycling, and disease transmission.
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http://dx.doi.org/10.1126/science.aam9712DOI Listing
January 2018

Social foraging and individual consistency in following behaviour: testing the information centre hypothesis in free-ranging vultures.

Proc Biol Sci 2017 Apr;284(1852)

Movement Ecology Lab, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Jerusalem 91904, Israel.

Uncertainties regarding food location and quality are among the greatest challenges faced by foragers and communal roosting may facilitate success through social foraging. The information centre hypothesis (ICH) suggests that uninformed individuals at shared roosts benefit from following informed individuals to previously visited resources. We tested several key prerequisites of the ICH in a social obligate scavenger, the Eurasian griffon vulture (), by tracking movements and behaviour of sympatric individuals over extended periods and across relatively large spatial scales, thereby precluding alternative explanations such as local enhancement. In agreement with the ICH, we found that 'informed' individuals returning to previously visited carcasses were followed by 'uninformed' vultures that consequently got access to these resources. When a dyad (two individuals that depart from the same roost within 2 min of each other) included an informed individual, they spent a higher proportion of the flight time close to each other at a shorter distance between them than otherwise. Although all individuals occasionally profited from following others, they differed in their tendencies to be informed or uninformed. This study provides evidence for 'following behaviour' in natural conditions and demonstrates differential roles and information states among foragers within a population. Moreover, demonstrating the possible reliance of vultures on following behaviour emphasizes that individuals in declining populations may suffer from reduced foraging efficiency.
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http://dx.doi.org/10.1098/rspb.2016.2654DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5394657PMC
April 2017

Decision-making by a soaring bird: time, energy and risk considerations at different spatio-temporal scales.

Philos Trans R Soc Lond B Biol Sci 2016 09;371(1704)

Movement Ecology Laboratory, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Jerusalem 91904, Israel.

Natural selection theory suggests that mobile animals trade off time, energy and risk costs with food, safety and other pay-offs obtained by movement. We examined how birds make movement decisions by integrating aspects of flight biomechanics, movement ecology and behaviour in a hierarchical framework investigating flight track variation across several spatio-temporal scales. Using extensive global positioning system and accelerometer data from Eurasian griffon vultures (Gyps fulvus) in Israel and France, we examined soaring-gliding decision-making by comparing inbound versus outbound flights (to or from a central roost, respectively), and these (and other) home-range foraging movements (up to 300 km) versus long-range movements (longer than 300 km). We found that long-range movements and inbound flights have similar features compared with their counterparts: individuals reduced journey time by performing more efficient soaring-gliding flight, reduced energy expenditure by flapping less and were more risk-prone by gliding more steeply between thermals. Age, breeding status, wind conditions and flight altitude (but not sex) affected time and energy prioritization during flights. We therefore suggest that individuals facing time, energy and risk trade-offs during movements make similar decisions across a broad range of ecological contexts and spatial scales, presumably owing to similarity in the uncertainty about movement outcomes.This article is part of the themed issue 'Moving in a moving medium: new perspectives on flight'.
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http://dx.doi.org/10.1098/rstb.2015.0397DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4992721PMC
September 2016

Extra-pair paternity in the socially monogamous white stork (Ciconia ciconia) is fairly common and independent of local density.

Sci Rep 2016 06 22;6:27976. Epub 2016 Jun 22.

Movement Ecology Laboratory, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, 91904, Jerusalem, Israel.

Although many birds are socially monogamous, most (>75%) studied species are not strictly genetically monogamous, especially under high breeding density. We used molecular tools to reevaluate the reproductive strategy of the socially monogamous white stork (Ciconia ciconia) and examined local density effects. DNA samples of nestlings (Germany, Spain) were genotyped and assigned relationships using a two-program maximum likelihood classification. Relationships were successfully classified in 79.2% of German (n = 120) and 84.8% of Spanish (n = 59) nests. For each population respectively, 76.8% (n = 73) and 66.0% (n = 33) of nests contained only full-siblings, 10.5% (n = 10) and 18.0% (n = 9) had half-siblings (at least one nestling with a different parent), 3.2% (n = 3) and 10.0% (n = 5) had unrelated nestlings (at least two nestlings, each with different parents), and 9.5% (n = 9) and 6.0% (n = 3) had "not full-siblings" (could not differentiate between latter two cases). These deviations from strict monogamy place the white stork in the 59(th) percentile for extra-pair paternity among studied bird species. Although high breeding density generally increases extra-pair paternity, we found no significant association with this species' mating strategies. Thus although genetic monogamy is indeed prominent in the white stork, extra-pair paternity is fairly common compared to other bird species and cannot be explained by breeding density.
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http://dx.doi.org/10.1038/srep27976DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4916429PMC
June 2016

Adult vultures outperform juveniles in challenging thermal soaring conditions.

Sci Rep 2016 06 13;6:27865. Epub 2016 Jun 13.

Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem Edmond J. Safra Campus, Jerusalem 91904, Israel.

Due to the potentially detrimental consequences of low performance in basic functional tasks, individuals are expected to improve performance with age and show the most marked changes during early stages of life. Soaring-gliding birds use rising-air columns (thermals) to reduce energy expenditure allocated to flight. We offer a framework to evaluate thermal soaring performance, and use GPS-tracking to study movements of Eurasian griffon vultures (Gyps fulvus). Because the location and intensity of thermals are variable, we hypothesized that soaring performance would improve with experience and predicted that the performance of inexperienced individuals (<2 months) would be inferior to that of experienced ones (>5 years). No differences were found in body characteristics, climb rates under low wind shear, and thermal selection, presumably due to vultures' tendency to forage in mixed-age groups. Adults, however, outperformed juveniles in their ability to adjust fine-scale movements under challenging conditions, as juveniles had lower climb rates under intermediate wind shear, particularly on the lee-side of thermal columns. Juveniles were also less efficient along the route both in terms of time and energy. The consequences of these handicaps are probably exacerbated if juveniles lag behind adults in finding and approaching food.
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http://dx.doi.org/10.1038/srep27865DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4904409PMC
June 2016

Novel Insights into the Map Stage of True Navigation in Nonmigratory Wild Birds (Stone Curlews, Burhinus oedicnemus).

Am Nat 2016 Jun 19;187(6):E152-65. Epub 2016 Apr 19.

In the map-and-compass model of true navigation, animals at unfamiliar sites determine their position relative to a destination site (the map stage) before progressing toward it (the compass stage). A major challenge in animal navigation research is to understand the still cryptic map stage in general and the map stage for free-ranging wild animals in particular. To address this challenge, we experimentally translocated wild, nonmigratory birds (stone curlews [Burhinus oedicnemus]) far from their nests and GPS-tracked their subsequent movements at high resolution and for long durations. Homing success was high and cannot be explained by random chance or landmark navigation, implying true navigation. Although highly motivated to return home, the homing trajectories of translocated birds exhibited a distinct, two-phase pattern resembling the map and compass stages: a long, tortuous wandering phase without consistent approach home, followed by a short and direct return phase. Birds retranslocated to the same site initially repeated the original wandering path but switched to the return phase earlier and after covering a smaller area; they returned home via a different path but with similar movement properties. We thus propose the map learning hypothesis, asserting that birds resolve the map by acquiring, potentially through learning, the relevant navigation cues during the wandering phase.
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http://dx.doi.org/10.1086/686054DOI Listing
June 2016

The challenges of the first migration: movement and behaviour of juvenile vs. adult white storks with insights regarding juvenile mortality.

J Anim Ecol 2016 07 19;85(4):938-47. Epub 2016 May 19.

Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, 91904, Jerusalem, Israel.

Migration conveys an immense challenge, especially for juvenile birds coping with enduring and risky journeys shortly after fledging. Accordingly, juveniles exhibit considerably lower survival rates compared to adults, particularly during migration. Juvenile white storks (Ciconia ciconia), which are known to rely on adults during their first fall migration presumably for navigational purposes, also display much lower annual survival than adults. Using detailed GPS and body acceleration data, we examined the patterns and potential causes of age-related differences in fall migration properties of white storks by comparing first-year juveniles and adults. We compared juvenile and adult parameters of movement, behaviour and energy expenditure (estimated from overall dynamic body acceleration) and placed this in the context of the juveniles' lower survival rate. Juveniles used flapping flight vs. soaring flight 23% more than adults and were estimated to expend 14% more energy during flight. Juveniles did not compensate for their higher flight costs by increased refuelling or resting during migration. When juveniles and adults migrated together in the same flock, the juvenile flew mostly behind the adult and was left behind when they separated. Juveniles showed greater improvement in flight efficiency throughout migration compared to adults which appears crucial because juveniles exhibiting higher flight costs suffered increased mortality. Our findings demonstrate the conflict between the juveniles' inferior flight skills and their urge to keep up with mixed adult-juvenile flocks. We suggest that increased flight costs are an important proximate cause of juvenile mortality in white storks and likely in other soaring migrants and that natural selection is operating on juvenile variation in flight efficiency.
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http://dx.doi.org/10.1111/1365-2656.12525DOI Listing
July 2016

Costs of migratory decisions: A comparison across eight white stork populations.

Sci Adv 2016 Jan 22;2(1):e1500931. Epub 2016 Jan 22.

Department of Migration and Immuno-Ecology, Max Planck Institute for Ornithology, 78315 Radolfzell, Germany.; Department of Biology, University of Konstanz, 78457 Konstanz, Germany.

Annual migratory movements can range from a few tens to thousands of kilometers, creating unique energetic requirements for each specific species and journey. Even within the same species, migration costs can vary largely because of flexible, opportunistic life history strategies. We uncover the large extent of variation in the lifetime migratory decisions of young white storks originating from eight populations. Not only did juvenile storks differ in their geographically distinct wintering locations, their diverse migration patterns also affected the amount of energy individuals invested for locomotion during the first months of their life. Overwintering in areas with higher human population reduced the stork's overall energy expenditure because of shorter daily foraging trips, closer wintering grounds, or a complete suppression of migration. Because migrants can change ecological processes in several distinct communities simultaneously, understanding their life history decisions helps not only to protect migratory species but also to conserve stable ecosystems.
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http://dx.doi.org/10.1126/sciadv.1500931DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4737271PMC
January 2016

Guidelines for Using Movement Science to Inform Biodiversity Policy.

Environ Manage 2015 Oct 23;56(4):791-801. Epub 2015 Jun 23.

National Environmental Research Program, Environmental Decisions Hub, Canberra, Australia,

Substantial advances have been made in our understanding of the movement of species, including processes such as dispersal and migration. This knowledge has the potential to improve decisions about biodiversity policy and management, but it can be difficult for decision makers to readily access and integrate the growing body of movement science. This is, in part, due to a lack of synthesis of information that is sufficiently contextualized for a policy audience. Here, we identify key species movement concepts, including mechanisms, types, and moderators of movement, and review their relevance to (1) national biodiversity policies and strategies, (2) reserve planning and management, (3) threatened species protection and recovery, (4) impact and risk assessments, and (5) the prioritization of restoration actions. Based on the review, and considering recent developments in movement ecology, we provide a new framework that draws links between aspects of movement knowledge that are likely the most relevant to each biodiversity policy category. Our framework also shows that there is substantial opportunity for collaboration between researchers and government decision makers in the use of movement science to promote positive biodiversity outcomes.
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http://dx.doi.org/10.1007/s00267-015-0570-5DOI Listing
October 2015

AcceleRater: a web application for supervised learning of behavioral modes from acceleration measurements.

Mov Ecol 2014 25;2(1):27. Epub 2014 Dec 25.

Movement Ecology Laboratory, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem, Israel.

Background: The study of animal movement is experiencing rapid progress in recent years, forcefully driven by technological advancement. Biologgers with Acceleration (ACC) recordings are becoming increasingly popular in the fields of animal behavior and movement ecology, for estimating energy expenditure and identifying behavior, with prospects for other potential uses as well. Supervised learning of behavioral modes from acceleration data has shown promising results in many species, and for a diverse range of behaviors. However, broad implementation of this technique in movement ecology research has been limited due to technical difficulties and complicated analysis, deterring many practitioners from applying this approach. This highlights the need to develop a broadly applicable tool for classifying behavior from acceleration data.

Description: Here we present a free-access python-based web application called AcceleRater, for rapidly training, visualizing and using models for supervised learning of behavioral modes from ACC measurements. We introduce AcceleRater, and illustrate its successful application for classifying vulture behavioral modes from acceleration data obtained from free-ranging vultures. The seven models offered in the AcceleRater application achieved overall accuracy of between 77.68% (Decision Tree) and 84.84% (Artificial Neural Network), with a mean overall accuracy of 81.51% and standard deviation of 3.95%. Notably, variation in performance was larger between behavioral modes than between models.

Conclusions: AcceleRater provides the means to identify animal behavior, offering a user-friendly tool for ACC-based behavioral annotation, which will be dynamically upgraded and maintained.
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http://dx.doi.org/10.1186/s40462-014-0027-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4337760PMC
February 2015

The gliding speed of migrating birds: slow and safe or fast and risky?

Ecol Lett 2014 Jun 18;17(6):670-9. Epub 2014 Mar 18.

Movement Ecology Laboratory, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, Edmond J. Safra campus, The Hebrew University of Jerusalem, 91904, Jerusalem, Israel.

Aerodynamic theory postulates that gliding airspeed, a major flight performance component for soaring avian migrants, scales with bird size and wing morphology. We tested this prediction, and the role of gliding altitude and soaring conditions, using atmospheric simulations and radar tracks of 1346 birds from 12 species. Gliding airspeed did not scale with bird size and wing morphology, and unexpectedly converged to a narrow range. To explain this discrepancy, we propose that soaring-gliding birds adjust their gliding airspeed according to the risk of grounding or switching to costly flapping flight. Introducing the Risk Aversion Flight Index (RAFI, the ratio of actual to theoretical risk-averse gliding airspeed), we found that inter- and intraspecific variation in RAFI positively correlated with wing loading, and negatively correlated with convective thermal conditions and gliding altitude, respectively. We propose that risk-sensitive behaviour modulates the evolution (morphology) and ecology (response to environmental conditions) of bird soaring flight.
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http://dx.doi.org/10.1111/ele.12268DOI Listing
June 2014

How fragmentation and corridors affect wind dynamics and seed dispersal in open habitats.

Proc Natl Acad Sci U S A 2014 Mar 24;111(9):3484-9. Epub 2014 Feb 24.

Department of Zoology, University of Wisconsin-Madison, Madison, WI 53706.

Determining how widespread human-induced changes such as habitat loss, landscape fragmentation, and climate instability affect populations, communities, and ecosystems is one of the most pressing environmental challenges. Critical to this challenge is understanding how these changes are affecting the movement abilities and dispersal trajectories of organisms and what role conservation planning can play in promoting movement among remaining fragments of suitable habitat. Whereas evidence is mounting for how conservation strategies such as corridors impact animal movement, virtually nothing is known for species dispersed by wind, which are often mistakenly assumed to not be limited by dispersal. Here, we combine mechanistic dispersal models, wind measurements, and seed releases in a large-scale experimental landscape to show that habitat corridors affect wind dynamics and seed dispersal by redirecting and bellowing airflow and by increasing the likelihood of seed uplift. Wind direction interacts with landscape orientation to determine when corridors provide connectivity. Our results predict positive impacts of connectivity and patch shape on species richness of wind-dispersed plants, which we empirically illustrate using 12 y of data from our experimental landscapes. We conclude that habitat fragmentation and corridors strongly impact the movement of wind-dispersed species, which has community-level consequences.
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http://dx.doi.org/10.1073/pnas.1308968111DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3948294PMC
March 2014

Factors influencing foraging search efficiency: why do scarce lappet-faced vultures outperform ubiquitous white-backed vultures?

Am Nat 2013 May 15;181(5):E102-15. Epub 2013 Mar 15.

Movement Ecology Laboratory, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, Hebrew University of Jerusalem, Givat Ram, Jerusalem 91904, Israel.

The search phase is a critical component of foraging behavior, affecting interspecific competition and community dynamics. Nevertheless, factors determining interspecific variation in search efficiency are still poorly understood. We studied differences in search efficiency between the lappet-faced vulture (Torgos tracheliotus; LFV) and the white-backed vulture (Gyps africanus; WBV) foraging on spatiotemporally unpredictable carcasses in Etosha National Park, Namibia. We used experimental food supply and high-resolution GPS tracking of free-ranging vultures to quantify search efficiency and elucidate the factors underlying the observed interspecific differences using a biased correlated random walk simulation model bootstrapped with the GPS tracking data. We found that LFV's search efficiency was higher than WBV's in both first-to-find, first-to-land, and per-individual-finding rate measures. Modifying species-specific traits in the simulation model allows us to assess the relative role of each factor in LFV's higher efficiency. Interspecific differences in morphology (through the effect on perceptual range and motion ability) and searchers' spatial dispersion (due to different roost arrangements) are in correspondence with the empirically observed advantage of LFV over WBV searchers, whereas differences in other aspects of the movement patterns appear to play a minor role. Our results provide mechanistic explanations for interspecific variation in search efficiency for species using similar resources and foraging modes.
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http://dx.doi.org/10.1086/670009DOI Listing
May 2013

Mixed strategies of griffon vultures' (Gyps fulvus) response to food deprivation lead to a hump-shaped movement pattern.

Mov Ecol 2013 5;1(1). Epub 2013 Jul 5.

Movement Ecology Laboratory, Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Edmond J. Safra Campus, Jerusalem, 91904 Israel.

Background: The need to obtain food is a critical proximate driver of an organism's movement that shapes the foraging and survival of individual animals. Consequently, the relationship between hunger and foraging has received considerable attention, leading to the common conception that hunger primarily enhances a "food-intake maximization" (FIMax) strategy and intensive search. A complementary explanation, however, suggests a trade-off with precautions taken to reduce the risk of physiological collapse from starvation, under a strategy we denote as "energy-expenditure minimization" (EEMin). The FImax-EEmin trade-off may interact with the forager's hunger level to shape a complex (non-monotonic) response pattern to increasing hunger. Yet, this important trade-off has rarely been investigated, particularly in free-ranging wild animals. We explored how hunger affects the movements of adult griffon vultures (Gyps fulvus) in southern Israel. Transmitters combining GPS and accelerometers provided high-resolution data on vultures' movements and behavior, enabling the identification of feeding events and the estimation of food deprivation periods (FDPs, measured in days), which is used as a proxy for hunger.

Results: Data from 47 vultures, tracked for 339 ± 36 days, reveal high variability in FDPs. While flight speed, flight straightness and the proportion of active flights were invariant in relation to food deprivation, a clear hump-shaped response was found for daily flight distances, maximal displacements and flight elevation. These movement characteristics increased during the first five days of the FDP sequence and decreased during the following five days. These characteristics also differed between short FDPs of up to four days, and the first four days of longer FDP sequences. These results suggest a switch from FIMax to EEMin strategies along the FDP sequence. They also indicate that vultures' response to hunger affected the eventual duration of the FDP. During winter (the vultures' incubation period characterized by unfavorable soaring meteorological conditions), the vultures' FIMax response was less intensive and resulted in longer starvation periods, while, in summer, more intensive FIMax response to hunger resulted in shorter FDPs.

Conclusions: Our results show a flexible, non-monotonic response of free-ranging wild animals to increasing hunger levels, reflecting a trade-off between increasing motivation to find food and the risk of starvation. The proposed trade-off offers a unifying perspective to apparently contradictory or case-specific empirical findings.
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http://dx.doi.org/10.1186/2051-3933-1-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4337378PMC
February 2015

A milestone for movement ecology research.

Mov Ecol 2013 3;1(1). Epub 2013 Jul 3.

Department of Engineering Mathematics and School of Biological Sciences, Bristol Centre for Complexity Sciences, University of Bristol, Bristol, BS8 1TR UK.

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http://dx.doi.org/10.1186/2051-3933-1-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4337752PMC
February 2015