A refined magnetic pulse treatment method for magnetic navigation experiments with adequate sham control: a case study on free-flying songbirds.

Migratory songbirds may navigate by extracting positional information from the geomagnetic field, potentially with a magnetic-particle-based receptor. Previous studies assessed this hypothesis experimentally by exposing birds to a strong but brief magnetic pulse aimed at remagnetizing the particles and evoking an altered behaviour. Critically, such studies were not ideally designed because they lacked an adequate sham treatment controlling for the induced electric field that is fundamentally associated with a magnetic pulse. Consequently, we designed a sham-controlled magnetic-pulse experiment, with sham and treatment pulse producing a similar induced electric field, while limiting the sham magnetic field to a value that is deemed insufficient to remagnetize particles. We tested this novel approach by pulsing more than 250 wild, migrating European robins (Erithacus rubecula) during two autumn seasons. After pulsing them, five traits of free-flight migratory behaviour were observed, but no effect of the pulse could be found. Notably, one of the traits, the migratory motivation of adults, was significantly affected in only one of the two study years. Considering the problem of reproducing experiments with wild animals, we recommend a multi-year approach encompassing large sample size, blinded design and built-in sham control to obtain future insights into the role of magnetic-particle-based magnetoreception in bird navigation.

A conceptual framework on the role of magnetic cues in songbird migration ecology.

Migrating animals perform astonishing seasonal movements by orienting and navigating over thousands of kilometres with great precision. Many migratory species use cues from the sun, stars, landmarks, olfaction and the Earth's magnetic field for this task. Among vertebrates, songbirds are the most studied taxon in magnetic-cue-related research. Despite multiple studies, we still lack a clear understanding of when, where and how magnetic cues affect the decision-making process of birds and hence, their realised migratory behaviour in the wild. This understanding is especially important to interpret the results of laboratory experiments in an ecologically appropriate way. In this review, we summarise the current findings about the role of magnetic cues for migratory decisions in songbirds. First, we review the methodological principles for orientation and navigation research, specifically by comparing experiments on caged birds with experiments on free-flying birds. While cage experiments can show the sensory abilities of birds, studies with free-flying birds can characterise the ecological roles of magnetic cues. Second, we review the migratory stages, from stopover to endurance flight, in which songbirds use magnetic cues for their migratory decisions and incorporate this into a novel conceptual framework. While we lack studies examining whether and when magnetic cues affect orientation or navigation decisions during flight, the role of magnetic cues during stopover is relatively well studied, but mostly in the laboratory. Notably, many such studies have produced contradictory results so that understanding the biological importance of magnetic cues for decisions in free-flying songbirds is not straightforward. One potential explanation is that reproducibility of magnetic-cue experiments is low, probably because variability in the behavioural responses of birds among experiments is high. We are convinced that parts of this variability can be explained by species-specific and context-dependent reactions of birds to the study conditions and by the bird's high flexibility in whether they include magnetic cues in a decision or not. Ultimately, this review should help researchers in the challenging field of magnetoreception to design experiments meticulously and interpret results of such studies carefully by considering the migration ecology of their focal species.

Eco-evolutionary drivers of avian migratory connectivity.

Migratory connectivity, reflecting the extent by which migrants tend to maintain their reciprocal positions in seasonal ranges, can assist in the conservation and management of mobile species, yet relevant drivers remain unclear. Taking advantage of an exceptionally large (~150,000 individuals, 83 species) and more-than-a-century-long dataset of bird ringing encounters, we investigated eco-evolutionary drivers of migratory connectivity in both short- and long-distance Afro-Palearctic migratory birds. Connectivity was strongly associated with geographical proxies of migration costs and was weakly influenced by biological traits and phylogeny, suggesting the evolutionary lability of migratory behaviour. The large intraspecific variability in avian migration strategies, through which most species geographically split into distinct migratory populations, explained why most of them were significantly connected. By unravelling key determinants of migratory connectivity, our study improves knowledge about the resilience of avian migrants to ecological perturbations, providing a critical tool to inform transboundary conservation and management strategies at the population level.

A magnetic pulse does not affect free-flight navigation behaviour of a medium-distance songbird migrant in spring.

Current evidence suggests that migratory animals extract map information from the geomagnetic field for true navigation. The sensory basis underlying this feat is elusive, but presumably involves magnetic particles. A common experimental manipulation procedure consists of pre-treating animals with a magnetic pulse, with the aim of re-magnetising particles to alter the internal representation of the external field prior to a navigation task. Although pulsing provoked deflected bearings in caged songbirds, analogous studies with free-flying songbirds yielded inconsistent results. Here, we pulsed European robins (Erithacus rubecula) at an offshore stopover site during spring migration and monitored their free-flight behaviour with a regional-scale network of radio-receiving stations. We found no pulse effect on departure probability, nocturnal departure timing departure direction or consistency of flight direction. This suggests either no use of the geomagnetic map by our birds, or that magnetic pulses do not affect the sensory system underlying geomagnetic map detection.

Transcriptome signature changes in the liver of a migratory passerine.

The liver plays a principal role in avian migration. Here, we characterised the liver transcriptome of a long-distance migrant, the Northern Wheatear (Oenanthe oenanthe), sampled at different migratory stages, looking for molecular processes linked with adaptations to migration. The analysis of the differentially expressed genes suggested changes in the periods of the circadian rhythm, variation in the proportion of cells in G1/S cell-cycle stages and the putative polyploidization of this cell population. This may explain the dramatic increment in the liver's metabolic capacities towards migration. Additionally, genes involved in anti-oxidative stress, detoxification and innate immune responses, lipid metabolism, inflammation and angiogenesis were regulated. Lipophagy and lipid catabolism were active at all migratory stages and increased towards the fattening and fat periods, explaining the relevance of lipolysis in controlling steatosis and maintaining liver health. Our study clears the way for future functional studies regarding long-distance avian migration.

No apparent effect of a magnetic pulse on free-flight behaviour in northern wheatears (Oenanthe oenanthe) at a stopover site.

Naïve migrants reach their wintering grounds following a clock-and-compass strategy. During these inaugural migrations, birds internalise, among others, cues from the Earth's magnetic field to create a geomagnetic map, with which they navigate to destinations familiar to them on subsequent migrations. Geomagnetic map cues are thought to be sensed by a magnetic-particle-based receptor, which can be specifically affected by a magnetic pulse. Indeed, the orientation of experienced but not naïve birds was compromised after magnetic pulsing, indicating geomagnetic map use. Little is known about the importance of this putative magnetoreceptor for navigation and decision-making in free-flying migrants. Therefore, we studied in unprecedented detail how a magnetic pulse would affect departure probability, nocturnal departure timing, departure direction and consistency in flight direction over 50-100 km in experienced and naïve long-distant migrant songbirds using a large-scale radio-tracking system. Contrary to our expectations and despite a high sample size (ntotal = 137) for a free-flight study, we found no significant after-effect of the magnetic pulse on the migratory traits, suggesting the geomagnetic map is not essential for the intermediate autumn migration phase. These findings warrant re-thinking about perception and use of geomagnetic maps for migratory decisions within a sensory and ecological context.

Days to visit an offshore island: effect of weather conditions on arrival fuel load and potential flight range for common blackbirds Turdus merula migrating over the North Sea.

BACKGROUND: Crossing open water instead of following the coast(line) is one way for landbirds to continue migration. However, depending on prevailing weather and the birds' physiological conditions, it is also a risky choice. To date, the question remains as to which interplay between environmental and physiological conditions force landbirds to stop on remote islands. We hypothesise that unfavourable winds affect lean birds with low energy resources, while poor visibility affects all birds regardless of their fuel loads. METHODS: To test this hypothesis, we caught 1312 common blackbirds Turdus merula stopping over on Helgoland during autumn and spring migration. Arrival fuel load was measured using quantitative magnetic resonance technology. Weather parameters (wind and relative humidity as a proxy for visibility) were interpolated for the night before arrival. Further, we calculated whether caught individuals would have successfully crossed the North Sea instead of landing on Helgoland, depending on wind conditions. RESULTS: Both wind and relative humidity the night before arrival were correlated with arrival fuel load. After nights with strong headwinds, birds caught the following day were mostly lean, most of which would not have managed to cross the sea if they had not stopped on Helgoland. In contrast, fat birds that could have successfully travelled on were caught mainly after nights with high relative humidity (≥ 80%). Furthermore, the rate of presumably successful flights was lower due to wind: although only 9% of all blackbirds captured on Helgoland had insufficient fuel loads to allow safe onward migration in still air, real wind conditions would have prevented 30% of birds from successfully crossing the sea during autumn and 21% during spring migration. CONCLUSIONS: We were able to decipher how physiological condition, wind and relative humidity partially force blackbirds to stop on a remote island. Adverse winds tend to affect lean birds with low energy resources, while poor visibility can affect blackbirds, regardless of whether the arrival fuel load was sufficient for onward flight. Our findings will help to understand different migratory strategies and explain further questions like migration timing.

The role of ketogenesis in the migratory fattening of the northern wheatear Oenanthe oenanthe.

The fuelling capacity of migratory birds and their ability to avoid health conditions derived from the subsequent fat overload are exceptional among vertebrates. In this work, we screen the expression of the genes involved in the production of ketone bodies (KB) in the liver of northern wheatears (Oenanthe oenanthe) during the development and resolution of migratory fattening. Thirteen genes were found to be regulated among the migratory stages. Based on the dynamics of gene expression, we concluded that KB play a versatile role in wheatears' energy metabolism homeostasis. The ketogenic pathway can adaptively: (i) provide carbon equivalents for lipogenesis, speeding up fuelling; (ii) replace glucose during long-distance flights using lipids as the substrate; (iii) act as a floodgate to avoid steatosis; and (iv) might provide a metabolic solution to defatting in captive birds.

The avian lightweights: Trans-Saharan migrants show lower lean body mass than short-/medium-distance migrants.

Avian trans-Saharan migrants travelling long distances and crossing ecological barriers experience different constraints in terms of time, energy and safety than short-/medium-distance migrants without barrier-crossings. As such, natural selection shapes the aerodynamic properties of these groups differently. Yet, to the best of our knowledge, we lack information on whether natural selection has contributed to reducing energetic flight costs through generally lower body mass in trans-Saharan migrants. To fill parts of this gap, we investigated this eco-morphological pattern in 5,410 individuals of 22 Palearctic songbird species ranging from short-/medium-distance to trans-Saharan migrants. We used individual size-independent scaled lean body mass values based on wing length as a measure of body size and, for the first time, precisely determined lean body mass values by direct measurements via quantitative magnetic resonance technology. Scaled lean body mass for a given body size was significantly higher in short-/medium-distance migrants than in trans-Saharan migrants. Although scaled lean body mass significantly decreased with increasing migration distance in short-/medium-distance migrants, no such effect was found in trans-Saharan migrants. Our results thus show an eco-morphological pattern relating species' lean body mass not only to migration distance but also to migration group. This suggests that selective effects of the presence/absence of ecological barriers and/or of a threshold level for migration distance on migrant birds may be more important than the linear continuum of migration distance per se.

Weather at the winter and stopover areas determines spring migration onset, progress, and advancements in Afro-Palearctic migrant birds.

Climate change causes changes in the timing of life cycle events across all trophic groups. Spring phenology has mostly advanced, but large, unexplained, variations are present between and within species. Each spring, migratory birds travel tens to tens of thousands of kilometers from their wintering to their breeding grounds. For most populations, large uncertainties remain on their exact locations outside the breeding area, and the time spent there or during migration. Assessing climate (change) effects on avian migration phenology has consequently been difficult due to spatial and temporal uncertainties in the weather potentially affecting migration timing. Here, we show for six trans-Saharan long-distance migrants that weather at the wintering and stopover grounds almost entirely (∼80%) explains interannual variation in spring migration phenology. Importantly, our spatiotemporal approach also allows for the systematic exclusion of influences at other locations and times. While increased spring temperatures did contribute strongly to the observed spring migration advancements over the 55-y study period, improvements in wind conditions, especially in the Maghreb and Mediterranean, have allowed even stronger advancements. Flexibility in spring migration timing of long-distance migrants to exogenous factors has been consistently underestimated due to mismatches in space, scale, time, and weather variable type.

Can Mitogenomes of the Northern Wheatear (Oenanthe oenanthe) Reconstruct Its Phylogeography and Reveal the Origin of Migrant Birds?

The Northern Wheatear (Oenanthe oenanthe, including the nominate and the two subspecies O. o. leucorhoa and O. o. libanotica) and the Seebohm's Wheatear (Oenanthe seebohmi) are today regarded as two distinct species. Before, all four taxa were regarded as four subspecies of the Northern Wheatear. Their classification has exclusively been based on ecological and morphological traits, while their molecular characterization is still missing. With this study, we used next-generation sequencing to assemble 117 complete mitochondrial genomes covering O. o. oenanthe, O. o. leucorhoa and O. seebohmi. We compared the resolution power of each individual mitochondrial marker and concatenated marker sets to reconstruct the phylogeny and estimate speciation times of three taxa. Moreover, we tried to identify the origin of migratory wheatears caught on Helgoland (Germany) and on Crete (Greece). Mitogenome analysis revealed two different ancient lineages that separated around 400,000 years ago. Both lineages consisted of a mix of subspecies and species. The phylogenetic trees, as well as haplotype networks are incongruent with the present morphology-based classification. Mitogenome could not distinguish these presumed species. The genetic panmixia among present populations and taxa might be the consequence of mitochondrial introgression between ancient wheatear populations.

Transcriptome signatures in the brain of a migratory songbird.

Most of the birds's adaptations for migration have a neuroendocrine origin, triggered by changes in photoperiod and the patterns of Earth's magnetic field. Migration phenomenology has been well described in the past decades, yet the genetic structure behind it remains terra incognita. We used RNA-Seq data to investigate which biological functions are linked with the seasonal brain adaptations of a long-distance trans-continental migratory passerine, the Northern Wheatear (Oenanthe oenanthe). We sequenced the wheatear's transcriptomes at three different stages: lean birds, a characteristic phenotype before the onset of migration, during fattening, and at their maximal migratory body mass. We identified a total of 15,357 genes in the brain of wheatears, of which 84 were differentially expressed. These were mostly related to nervous tissue development, angiogenesis, ATP production, innate immune response, and antioxidant protection, as well as GABA and dopamine signalling. The expression pattern of differentially expressed genes is correlated with typical phenotypic changes before migration, such as hyperphagia, migratory restlessness, and a potential increment in the visual and spatial memory capacities. Our work points out, for future studies, biological functions found to be involved in the development of the migratory phenotype -a unique model to study the core of neural, energetic and muscular adaptations for endurance exercise. Comparison of wheatears' transcriptomic data with two other studies with similar goals shows no correlation among the trends in the gene expression. It highlights the complexity and diversity of adaptations for long-distance migration in birds.

Assortative mating frames establishment in a young island bird population.

Successful island colonizations are key events to understand range dynamic processes, but studying a young population right after it reaches establishment is a rare opportunity in natural systems. The genetic structure of a recently established population may offer unique insights into its colonization history and demographic processes that are important for a successful colonization. Here, we studied the population genetics of a recently established island population of Eurasian blackbirds (Aves: Turdus merula) located on the island of Heligoland in the German North Sea. Using microsatellites, we genotyped the majority of the island population, including the nestlings, over a 4-year period between 2004 and 2007. We also genotyped high numbers of migrants on stopover and mainland individuals, as they are potential founders of the island population. We identified two genetic clusters that comply with the migrating and mainland birds. While most of the island birds belong to the mainland cluster, some breeding individuals and a low fraction of the offspring belong to the genetic cluster found in migrating individuals with almost no admixture between the two, pointing to assortative mating acting on the island population. We did not find any evidence for founder events and detected deviations from the Hardy-Weinberg equilibrium that disappeared in cohorts of older age that coincide with a lower number of siblings in older cohorts. The observed genetic patterns unravel a complex colonization history to which migratory and mainland birds have contributed and which is characterized by assortative mating. Further research will be directed towards habitat selection and phenotypic differences as potential drivers of assortative mating in this island population.

Autumn bird migration phenology: A potpourri of wind, precipitation and temperature effects.

Climate change has caused a clear and univocal trend towards advancement in spring phenology. Changes in autumn phenology are much more diverse, with advancement, delays, and 'no change' all occurring frequently. For migratory birds, patterns in autumn migration phenology trends have been identified based on ecological and life-history traits. Explaining interspecific variation has nevertheless been challenging, and the underlying mechanisms have remained elusive. Radar studies on non-species-specific autumn migration intensity have repeatedly suggested that there are strong links with weather. In long-term species-specific studies, the variance in autumn migration phenology explained by weather has, nevertheless, been rather low, or a relationship was even lacking entirely. We performed a spatially explicit time window analysis of weather effects on mean autumn passage of four trans-Saharan and six intra-European passerines to gain insights into this apparent contradiction. We analysed data from standardized daily captures at the Heligoland island constant-effort site (Germany), in combination with gridded daily temperature, precipitation and wind data over a 55-year period (1960-2014), across northern Europe. Weather variables at the breeding and stopover grounds explained up to 80% of the species-specific interannual variability in autumn passage. Overall, wind conditions were most important. For intra-European migrants, wind was even twice as important as either temperature or precipitation, and the pattern also held in terms of relative contributions of each climate variable to the temporal trends in autumn phenology. For the trans-Saharan migrants, however, the pattern of relative trend contributions was completely reversed. Temperature and precipitation had strong trend contributions, while wind conditions had only a minor impact because they did not show any strong temporal trends. As such, understanding species-specific effects of climate on autumn phenology not only provides unique insights into each species' ecology but also how these effects shape the observed interspecific heterogeneity in autumn phenological trends.

Unravelling migration connectivity reveals unsustainable hunting of the declining ortolan bunting.

In France, illegal hunting of the endangered ortolan bunting Emberiza hortulana has been defended for the sake of tradition and gastronomy. Hunters argued that ortolan buntings trapped in southwest France originate from large and stable populations across the whole of Europe. Yet, the European Commission referred France to the Court of Justice of the European Union (EU) in December 2016 for infringements to legislation (IP/16/4213). To better assess the impact of hunting in France, we combined Pan-European data from archival light loggers, stable isotopes, and genetics to determine the migration strategy of the species across continents. Ortolan buntings migrating through France come from northern and western populations, which are small, fragmented and declining. Population viability modeling further revealed that harvesting in southwest France is far from sustainable and increases extinction risk. These results provide the sufficient scientific evidence for justifying the ban on ortolan harvesting in France.

An exception to the rule: Captivity does not stress wild migrating northern wheatears.

Wild animals typically suffer from stress when brought into captivity. This stress is characterized by elevated circulating glucocorticoid levels and weight loss. We here describe for the first time a case where a wild animal, the long-distance migrating northern wheatear, does not show signs of stress when caged. We captured these birds on a stopover site during their spring migration and caged them individually with ad libitum access to food and water. The birds were divided into four groups and were blood-sampled immediately in the field, a few hours after caging, one day after caging, or three days after caging, respectively. From these blood-samples we determined circulating corticosterone level. Food intake and body mass were also monitored. We found that, with very few exceptions, corticosterone levels were low and did not differ among the groups. Accordingly, almost all birds consumed huge quantities of food and substantially increased their body mass. Together these results clearly show that caging does not result in indications of stress in wild migrating northern wheatears. Confinement-specific conditions such as restricted movement normally stress animals. We suggest migratory birds may not perceive such conditions as stressors due to their hyperphagic state, a notion that requires further testing.

De novo annotation of the transcriptome of the Northern Wheatear (Oenanthe oenanthe).

We have sequenced a partial transcriptome of the Northern Wheatear (Oenanthe oenanthe), a species with one of the longest migrations on Earth. The transcriptome was constructed de novo using RNA-Seq sequence data from the pooled mRNA of six different tissues: brain, muscle, intestine, liver, adipose tissue and skin. The samples came from nine captive-bred wheatears collected at three different stages of the endogenous autumn migratory period: (1) lean birds prior the onset of migration, (2) during the fattening stage and (3) individuals at their migratory body mass plateau, when they have almost doubled their lean body mass. The sample structure used to build up the transcriptome of the Northern Wheatears concerning tissue composition and time guarantees the future survey of the regulatory genes involved in the development of the migratory phenotype. Through the pre-migratory period, birds accomplish outstanding physical and behavioural changes that involve all organ systems. Nevertheless, the molecular mechanisms through which birds synchronize and control hyperphagia, fattening, restlessness increase, immunity boosting and tuning the muscles for such endurance flight are still largely unknown. The use of RNA-Seq has emerged as a powerful tool to analyse complex traits on a broad scale, and we believe it can help to characterize the migratory phenotype of wheatears at an unprecedented level. The primary challenge to conduct quantitative transcriptomic studies in non-model species is the availability of a reference transcriptome, which we have constructed and described in this paper. The cDNA was sequenced by pyrosequencing using the Genome Sequencer Roche GS FLX System; with single paired-end reads of about 400 bp. We estimate the total number of genes at 15,640, of which  67% could be annotated using Turkey and Zebra Finch genomes, or protein sequence information from SwissProt and NCBI databases. With our study, we have made a first step towards understanding the migratory phenotype regarding gene expression of a species that has become a model to study birds long-distance migrations.

Migration phenology determines niche use of East Asian buntings (Emberizidae) during stopover.

Stopover niche utilization of birds during migration has not gained much attention so far, since the majority of the studies focuses on breeding or wintering areas. However, stopover sites are crucial for migratory birds. They are often used by a multitude of species, which could lead to increased competition. In this work, we investigated niche use of 8 migratory and closely related Emberiza bunting species at a stopover site in Far East Russia, situated on the poorly studied East Asian flyway. We used bird ringing data to evaluate morphological similarity as well as niche overlap on the trophic, spatial, and temporal dimension. Bill morphology was used as a proxy for their trophic niche. We were able to prove that a majority of the species occupies well-defined stopover niches on at least one of the dimensions. Niche breadth and niche overlap differ between spring and autumn season with higher overlap found during spring. Morphological differences are mostly related to overall size and wing pointedness. The temporal dimension is most important for segregation among the studied species. Furthermore, all species seem to exhibit a rather strict and consistent phenological pattern. Their occurrence at the study site is highly correlated with their geographic origin and the length of their migration route. We assume that buntings are able to use available resources opportunistically during stopover, while trying to follow a precise schedule in order to avoid competition and to ensure individual fitness.

The influence of weather on avian spring migration phenology: What, where and when?

Over the past decades, spring arrival and passage of most short- and medium-distance migrating birds in the Northern Hemisphere have advanced. Changes in spring temperature at the passage or arrival area have been most frequently shown to be related to these changes in spring migration phenology. In most studies, preliminary assumptions are made on both the spatial location and the specific time frame of the weather influencing spring migration phenology. We performed a spatially explicit time-window analysis of the effect of weather on mean spring passage dates of nine short- and medium-distance passerines. We analysed data from standardized daily captures at the Helgoland (Germany) constant-effort site, in combination with gridded daily temperature, precipitation and wind data from the NCEP data set over a 55-year period (1960-2014), across the whole of West Europe and North Africa. Although we allowed for a time window of any length at any location, nevertheless incorporating various measures to avoid spurious correlations, time windows at the likely wintering or spring stopover grounds were almost exclusively selected as the best predicting variables (96%-100% of identified variables). The weather variables at the wintering and stopover grounds explain up to 77% of the interannual variability in spring passage. Yet, the response of spring migration phenology to weather at the winter or stopover areas does not fully explain the observed trends. Spring migration phenology is, hence, strongly driven by weather at the wintering and stopover grounds, but additional mechanisms are needed to fully explain the advancement of spring migration. Our results also clearly show that previously illustrated correlations, or the lack thereof, between spring migration phenology and weather at the passage or arrival location are due to spatio-temporal correlations in the weather data. This spatial mismatch might have led to false conclusions, especially the further away the wintering or stopover sites are.

Challenging a 15-year-old claim: The North Atlantic Oscillation index as a predictor of spring migration phenology of birds.

Many migrant bird species that breed in the Northern Hemisphere show advancement in spring arrival dates. The North Atlantic Oscillation (NAO) index is one of the climatic variables that have been most often investigated and shown to be correlated with these changes in spring arrival. Although the NAO is often claimed to be a good predictor or even to have a marked effect on interannual changes in spring migration phenology of Northern Hemisphere breeding birds, the results on relations between spring migration phenology and NAO show a large variety, ranging from no, over weak, to a strong association. Several factors, such as geographic location, migration phase, and the NAO index time window, have been suggested to partly explain these observed differences in association. A combination of a literature meta-analysis, and a meta-analysis and sliding time window analysis of a dataset of 23 short- and long-distance migrants from the constant-effort trapping garden at Helgoland, Germany, however, paints a completely different picture. We found a statistically significant overall effect size of the NAO on spring migration phenology (coefficient = -0.14, SE = 0.054), but this on average only explains 0%-6% of the variance in spring migration phenology across all species. As such, the value and biological meaning of the NAO as a general predictor or explanatory variable for climate change effects on migration phenology of birds, seems highly questionable. We found little to no definite support for previously suggested factors, such as geographic location, migration phenology phase, or the NAO time window, to explain the heterogeneity in correlation differences. We, however, did find compelling evidence that the lack of accounting for trends in both time series has led to strongly inflated (spurious) correlations in many studies (coefficient = -0.13, SE = 0.019).