Learning shapes the development of migratory behavior.

How animals refine migratory behavior over their lifetime (i.e., the ontogeny of migration) is an enduring question with important implications for predicting the adaptive capacity of migrants in a changing world. Yet, our inability to monitor the movements of individuals from early life onward has limited our understanding of the ontogeny of migration. The exploration-refinement hypothesis posits that learning shapes the ontogeny of migration in long-lived species, resulting in greater exploratory behavior early in life followed by more rapid and direct movement during later life. We test the exploration-refinement hypothesis by examining how white storks (Ciconia ciconia) balance energy, time, and information as they develop and refine migratory behavior during the first years of life. Here, we show that young birds reduce energy expenditure during flight while also increasing information gain by exploring new places during migration. As the birds age and gain more experience, older individuals stop exploring new places and instead move more quickly and directly, resulting in greater energy expenditure during migratory flight. During spring migration, individuals innovated novel shortcuts during the transition from early life into adulthood, suggesting a reliance on spatial memory acquired through learning. These incremental refinements in migratory behavior provide support for the importance of individual learning within a lifetime in the ontogeny of long-distance migration.

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.

Growth of non-English-language literature on biodiversity conservation.

English is widely recognized as the language of science, and English-language publications (ELPs) are rapidly increasing. It is often assumed that the number of non-ELPs is decreasing. This assumption contributes to the underuse of non-ELPs in conservation science, practice, and policy, especially at the international level. However, the number of conservation articles published in different languages is poorly documented. Using local and international search systems, we searched for scientific articles on biodiversity conservation published from 1980 to 2018 in English and 15 non-English languages. We compared the growth rate in publications across languages. In 12 of the 15 non-English languages, published conservation articles significantly increased every year over the past 39 years, at a rate similar to English-language articles. The other three languages showed contrasting results, depending on the search system. Since the 1990s, conservation science articles in most languages increased exponentially. The variation in the number of non-English-language articles identified among the search systems differed markedly (e.g., for simplified Chinese, 11,148 articles returned with local search system and 803 with Scopus). Google Scholar and local literature search systems returned the most articles for 11 and 4 non-English languages, respectively. However, the proportion of peer-reviewed conservation articles published in non-English languages was highest in Scopus, followed by Web of Science and local search systems, and lowest in Google Scholar. About 20% of the sampled non-English-language articles provided no title or abstract in English; thus, in theory, they were undiscoverable with English keywords. Possible reasons for this include language barriers and the need to disseminate research in countries where English is not widely spoken. Given the known biases in statistical methods and study characteristics between English- and non-English-language studies, non-English-language articles will continue to play an important role in improving the understanding of biodiversity and its conservation.

RESUMEN: El inglés es reconocido como el idioma de la ciencia y las publicaciones en inglés (PI) cada vez son más. Con frecuencia se asume que el número de publicaciones en idiomas diferentes al inglés está disminuyendo. Esta suposición contribuye al uso reducido de las publicaciones que no están en inglés en las ciencias, prácticas y políticas de la conservación, especialmente a nivel internacional. Sin embargo, el número de artículos de conservación publicados en diferentes idiomas está muy mal documentado. Usamos sistemas de búsqueda locales e internacionales para buscar artículos científicos sobre la conservación de la biodiversidad publicados entre 1980 y 2018 en inglés y en quince idiomas diferentes al inglés. También comparamos la tasa de incremento de publicaciones en los diferentes idiomas. En doce de los quince idiomas diferentes al inglés, los artículos de conservación publicados incrementaron significativamente cada año durante los últimos 39 años, una tasa similar a los artículos en inglés. Los otros tres idiomas mostraron resultados contrastantes según el sistema de búsqueda. Desde la década de 1990, los artículos sobre ciencias de la conservación incrementaron exponencialmente en la mayoría de los idiomas. La variación en el número de artículos identificados en idiomas diferentes al inglés difirió notablemente de acuerdo con los sistemas de búsqueda (p. ej.: en el caso del chino simplificado, obtuvimos 11,148 artículos con el sistema de búsqueda local y 803 con Scopus). Google Scholar y los sistemas locales de búsqueda arrojaron la mayor cantidad de artículos en 11 y 4 idiomas diferentes al inglés, respectivamente. Sin embargo, la proporción de artículos sobre conservación revisados por pares y publicados en idiomas diferentes al inglés fue mayor en Scopus, seguida por Web of Science y los sistemas locales de búsqueda, con la menor proporción en Google Scholar. Aproximadamente el 20% de la muestra de artículos en idiomas diferentes al inglés no contaban con título o con resumen en inglés; por lo tanto, en teoría, eran imposibles de encontrar mediante palabras clave en inglés. Las posibles explicaciones de esto incluyen las barreras del idioma y la necesidad de difundir la investigación en países en los que el inglés no se habla extensamente. Con los sesgos conocidos de los métodos estadísticos y de las características de estudio entre los trabajos en inglés y en otros idiomas, los artículos en idiomas diferentes al inglés seguirán desempeñando un papel importante en el entendimiento de la biodiversidad y su conservación. Incremento de la Literatura sobre la Conservación de la Biodiversidad en Idiomas Diferentes al Inglés.

The interplay of wind and uplift facilitates over-water flight in facultative soaring birds.

Flying over the open sea is energetically costly for terrestrial birds. Despite this, over-water journeys of many birds, sometimes hundreds of kilometres long, are uncovered by bio-logging technology. To understand how these birds afford their flights over the open sea, we investigated the role of atmospheric conditions, specifically wind and uplift, in subsidizing over-water flight at a global scale. We first established that ΔT, the temperature difference between sea surface and air, is a meaningful proxy for uplift over water. Using this proxy, we showed that the spatio-temporal patterns of sea-crossing in terrestrial migratory birds are associated with favourable uplift conditions. We then analysed route selection over the open sea for five facultative soaring species, representative of all major migratory flyways. The birds maximized wind support when selecting their sea-crossing routes and selected greater uplift when suitable wind support was available. They also preferred routes with low long-term uncertainty in wind conditions. Our findings suggest that, in addition to wind, uplift may play a key role in the energy seascape for bird migration that in turn determines strategies and associated costs for birds crossing ecological barriers such as the open sea.

Climate change alters the optimal wind-dependent flight routes of an avian migrant.

Migratory birds can be adversely affected by climate change as they encounter its geographically uneven impacts in various stages of their life cycle. While a wealth of research is devoted to the impacts of climate change on distribution range and phenology of migratory birds, the indirect effects of climate change on optimal migratory routes and flyways, through changes in air movements, are poorly understood. Here, we predict the influence of climate change on the migratory route of a long-distant migrant using an ensemble of correlative modelling approaches, and present and future atmospheric data obtained from a regional climate model. We show that changes in wind conditions by mid-century will result in a slight shift and reduction in the suitable areas for migration of the study species, the Oriental honey-buzzard, over a critical section of its autumn journey, followed by a complete loss of this section of the traditional route by late century. Our results highlight the need for investigating the consequences of climate change-induced disturbance in wind support for long-distance migratory birds, particularly species that depend on the wind to cross ecological barriers, and those that will be exposed to longer journeys due to future range shifts.

Experience reduces route selection for conspecifics by the collectively migrating white stork.

Migration can be an energetically costly behavior with strong fitness consequences in terms of mortality and reproduction.1,2,3,4,5,6,7,8,9,10,11 Migrants should select migratory routes to minimize their costs, but both costs and benefits may change with experience.12,13,14 This raises the question of whether experience changes how individuals select their migratory routes. Here, we investigate the effect of age on route selection criteria in a collectively migrating soaring bird, the white stork (Ciconia ciconia). We perform step-selection analysis on a longitudinal dataset tracking 158 white storks over up to 9 years to quantify how they select their routes based on the social and atmospheric environments and to examine how this selection changes with age. We find clear ontogenetic shifts in route selection criteria. Juveniles choose routes that have good atmospheric conditions and high conspecific densities. Yet, as they gain experience, storks' selection on the availability of social information reduces-after their fifth migration, experienced birds also choose routes with low conspecific densities. Thus, our results suggest that as individuals age, they gradually replace information gleaned from other individuals with information gained from experience, allowing them to shift their migration timing and increasing the timescale at which they select their routes.

Developmental stage shapes the realized energy landscape for a flight specialist.

The heterogeneity of the physical environment determines the cost of transport for animals, shaping their energy landscape. Animals respond to this energy landscape by adjusting their distribution and movement to maximize gains and reduce costs. Much of our knowledge about energy landscape dynamics focuses on factors external to the animal, particularly the spatio-temporal variations of the environment. However, an animal's internal state can significantly impact its ability to perceive and utilize available energy, creating a distinction between the 'fundamental' and the 'realized' energy landscapes. Here, we show that the realized energy landscape varies along the ontogenetic axis. Locomotor and cognitive capabilities of individuals change over time, especially during the early life stages. We investigate the development of the realized energy landscape in the Central European Alpine population of the golden eagle Aquila chrysaetos, a large predator that requires negotiating the atmospheric environment to achieve energy-efficient soaring flight. We quantified weekly energy landscapes using environmental features for 55 juvenile golden eagles, demonstrating that energetic costs of traversing the landscape decreased with age. Consequently, the potentially flyable area within the Alpine region increased 2170-fold during their first three years of independence. Our work contributes to a predictive understanding of animal movement by presenting ontogeny as a mechanism shaping the realized energy landscape.

Seabird morphology determines operational wind speeds, tolerable maxima, and responses to extremes.

Storms can cause widespread seabird stranding and wrecking,1,2,3,4,5 yet little is known about the maximum wind speeds that birds are able to tolerate or the conditions they avoid. We analyzed >300,000 h of tracking data from 18 seabird species, including flapping and soaring fliers, to assess how flight morphology affects wind selectivity, both at fine scales (hourly movement steps) and across the breeding season. We found no general preference or avoidance of particular wind speeds within foraging tracks. This suggests seabird flight morphology is adapted to a "wind niche," with higher wing loading being selected in windier environments. In support of this, wing loading was positively related to the median wind speeds on the breeding grounds, as well as the maximum wind speeds in which birds flew. Yet globally, the highest wind speeds occur in the tropics (in association with tropical cyclones) where birds are morphologically adapted to low median wind speeds. Tropical species must therefore show behavioral responses to extreme winds, including long-range avoidance of wind speeds that can be twice their operable maxima. By contrast, Procellariiformes flew in almost all wind speeds they encountered at a seasonal scale. Despite this, we describe a small number of cases where albatrosses avoided strong winds at close range, including by flying into the eye of the storm. Extreme winds appear to pose context-dependent risks to seabirds, and more information is needed on the factors that determine the hierarchy of risk, given the impact of global change on storm intensity.6,7.

Experience does not change the importance of wind support for migratory route selection by a soaring bird.

Migration is a complex behaviour that is costly in terms of time, energy and risk of mortality. Thermal soaring birds rely on airflow, specifically wind support and uplift, to offset their energetic costs of flight. Their migratory routes are a record of movement decisions to negotiate the atmospheric environment and achieve efficiency. We expected that, regardless of age, birds use wind support to select their routes. Because thermal soaring is a complex flight behaviour that young birds need to learn, we expected that, as individuals gain more experience, their movement decisions will also increasingly favour the best thermal uplift conditions. We quantified how route choice during autumn migration of young European honey buzzards (Pernis apivorus) was adjusted to wind support and uplift over up to 4 years of migration and compared this with the choices of adult birds. We found that wind support was important in all migrations. However, we did not find an increase in the use of thermal uplifts. This could be due to the species-specific learning period and/or an artefact of the spatio-temporal scale of our uplift proxies.

New frontiers in bird migration research.

Bird migrations are impressive behavioral phenomena, representing complex spatiotemporal strategies to balance costs of living while maximizing fitness. The field of bird migration research has made great strides over the past decades, yet fundamental gaps remain. Technologies have sparked a transformation in the study of bird migration research by revealing remarkable insights into the underlying behavioral, cognitive, physiological and evolutionary mechanisms of these diverse journeys. Here, we aim to encourage broad discussions and promote future studies by highlighting research fields that are characterized by major knowledge gaps or conflicting evidence, namely the fields of navigation, social learning, individual development, energetics and conservation. We approach each topic by summarizing the current state of knowledge and provide a future outlook of ideas and state-of-the-art methods to further advance the field. Integrating knowledge across these disciplines will allow us to understand the adaptive abilities of different species and to develop effective conservation strategies in a rapidly changing world.

Raptor migration in an oceanic flyway: wind and geography shape the migratory route of grey-faced buzzards in East Asia.

Flapping flight is relatively costly for soaring birds such as raptors. To avoid costly flight, migrating raptors generally avoid flying over water. As a result, all but one of the global raptor migration flyways are largely over land. The East Asian oceanic flyway for raptors is the exception. Raptor species using this flyway migrate by island-hopping, flying over open ocean for distances of up to 300 km between islands. We used satellite telemetry data for grey-faced buzzards Butastur indicus, a species that dominates the southern part of the flyway, to investigate the geographical and atmospheric factors responsible for the suitability of this flyway for raptor migration. Using a combination of least-cost path analysis and a step selection function, we found that the occurrence of numerous islands and also suitable wind support along the oceanic flyway are responsible for route selection in grey-faced buzzards. These results confirm the role of islands, but also wind, in shaping the East Asian oceanic flyway of long-distance raptor migration.

Upward Altitudinal Shifts in Habitat Suitability of Mountain Vipers since the Last Glacial Maximum.

We determined the effects of past and future climate changes on the distribution of the Montivipera raddei species complex (MRC) that contains rare and endangered viper species limited to Iran, Turkey and Armenia. We also investigated the current distribution of MRC to locate unidentified isolated populations as well as to evaluate the effectiveness of the current network of protected areas for their conservation. Present distribution of MRC was modeled based on ecological variables and model performance was evaluated by field visits. Some individuals at the newly identified populations showed uncommon morphological characteristics. The distribution map of MRC derived through modeling was then compared with the distribution of protected areas in the region. We estimated the effectiveness of the current protected area network to be 10%, which would be sufficient for conserving this group of species, provided adequate management policies and practices are employed. We further modeled the distribution of MRC in the past (21,000 years ago) and under two scenarios in the future (to 2070). These models indicated that climatic changes probably have been responsible for an upward shift in suitable habitats of MRC since the Last Glacial Maximum, leading to isolation of allopatric populations. Distribution will probably become much more restricted in the future as a result of the current rate of global warming. We conclude that climate change most likely played a major role in determining the distribution pattern of MRC, restricting allopatric populations to mountaintops due to habitat alterations. This long-term isolation has facilitated unique local adaptations among MRC populations, which requires further investigation. The suitable habitat patches identified through modeling constitute optimized solutions for inclusion in the network of protected areas in the region.

Is black coat color in wolves of Iran an evidence of admixed ancestry with dogs?

Melanism is not considered a typical characteristic in wolves of Iran and dark wolves are believed to have originated from crossbreeding with dogs. Such hybrid individuals can be identified with the combined use of genetic and morphological markers. We analyzed two black wolves using a 544 base pairs (bp) fragment of the mtDNA control region and 15 microsatellite loci in comparison with 28 dogs, 28 wolves, and four known hybrids. The artificial neural networks (ANNs) method was applied to microsatellite data to separate genetically differentiated samples of wolves, dogs, and hybrids, and to determine the correct class for the black specimens. Individual assignments based on ANNs showed that black samples were genetically closer to wolves. Also, in the neighbor-joining network of mtDNA haplotypes, wolves and dogs were separated, with the dark specimens located in the wolf branch as two separate haplotypes. Furthermore, we compared 20 craniometrical characters of the two black individuals with 14 other wolves. The results showed that craniometrical measures of the two black wolves fall within the range of wolf skulls. We found no trace of recent hybridization with free-ranging dogs in the two black wolves. Dark coat color might be the result of a natural combination of alleles in the coat-color-determining gene, mutation in the K locus due to past hybridization with free-ranging dogs, or the effect of ecological factors and adaption to habitat conditions.