White-crested elaenias (Elaenia albiceps chilensis) breeding across Patagonia exhibit similar spatial and temporal movement patterns throughout the year.

For migratory birds, events happening during any period of their annual cycle can have strong carry-over effects on the subsequent periods. The strength of carry-over effects between non-breeding and breeding grounds can be shaped by the degree of migratory connectivity: whether or not individuals that breed together also migrate and/or spend the non-breeding season together. We assessed the annual cycle of the White-crested Elaenia (Elaenia albiceps chilensis), the longest-distance migrant flycatcher within South America, which breeds in Patagonia and spends the non-breeding season as far north as Amazonia. Using light-level geolocators, we tracked the annual movements of elaenias breeding on southern Patagonia and compared it with movements of elaenias breeding in northern Patagonia (1,365 km north) using Movebank Repository data. We found that elaenias breeding in southern Patagonia successively used two separate non-breeding regions while in their Brazilian non-breeding grounds, as already found for elaenias breeding in the northern Patagonia site. Elaenias breeding in both northern and southern Patagonia also showed high spread in their non-breeding grounds, high non-breeding overlap among individuals from both breeding sites, and similar migration phenology, all of which suggests weak migratory connectivity for this species. Elucidating the annual cycle of this species, with particular emphasis on females and juveniles, still requires further research across a wide expanse of South America. This information will be critical to understanding and possibly predicting this species' response to climate change and rapid land-use changes.

Flexibility underlies differences in mitochondrial respiratory performance between migratory and non-migratory White-crowned Sparrows (Zonotrichia leucophrys).

Migration is one of the most energy-demanding behaviors observed in birds. Mitochondria are the primary source of energy used to support these long-distance movements, yet how mitochondria meet the energetic demands of migration is scarcely studied. We quantified changes in mitochondrial respiratory performance in the White-crowned Sparrow (Zonotrichia leucophrys), which has a migratory and non-migratory subspecies. We hypothesized that the long-distance migratory Gambel's subspecies (Z. l. gambelii) would show higher mitochondrial respiratory performance compared to the non-migratory Nuttall's subspecies (Z. l. nuttalli). We sampled Gambel's individuals during spring pre-migration, active fall migration, and a period with no migration or breeding (winter). We sampled Nuttall's individuals during periods coinciding with fall migration and the winter period of Gambel's annual cycle. Overall, Gambel's individuals had higher citrate synthase, a proxy for mitochondrial volume, than Nuttall's individuals. This was most pronounced prior to and during migration. We found that both OXPHOS capacity (state 3) and basal respiration (state 4) of mitochondria exhibit high seasonal flexibility within Gambel's individuals, with values highest during active migration. These values in Nuttall's individuals were most similar to Gambel's individuals in winter. Our observations indicate that seasonal changes in mitochondrial respiration play a vital role in migration energetics.

Responses in the breeding parameters of the collared flycatcher to the changing climate.

Global climate change involves various aspects of climate, including precipitation changes and declining surface wind speeds, but studies investigating biological responses have often focused on the impacts of rising temperatures. Additionally, related long-term studies on bird reproduction tend to concentrate on breeding onset, even though other aspects of breeding could also be sensitive to the diverse weather aspects. This study aimed to explore how multiple aspects of breeding (breeding onset, hatching delay, breeding season length, clutch size, fledgling number) were associated with different weather components. We used an almost four-decade-long dataset to investigate the various aspects of breeding parameters of a collared flycatcher (Ficedula albicollis) population in the Carpathian Basin. Analyses revealed some considerable associations, for example, breeding seasons lengthened with the amount of daily precipitation, and clutch size increased with the number of cool days. Parallel and opposing changes in the correlated pairs of breeding and weather parameters were also observed. The phenological mismatch between prey availability and breeding time slightly increased, and fledgling number strongly decreased with increasing mistiming. Our results highlighted the intricate interplay between climate change and the reproductive patterns of migratory birds, emphasizing the need for a holistic approach. The results also underscored the potential threats posed by climate change to bird populations and the importance of adaptive responses to changing environmental conditions.

Night-time neuronal activation of Cluster N in a North American songbird.

Night-migrating songbirds utilize the Earth's magnetic field to help navigate to and from their breeding sites each year. A region of the avian forebrain called Cluster N has been shown to be activated during night migratory behavior and it has been implicated in processing geomagnetic information. Previous studies with night-migratory European songbirds have shown that neuronal activity at Cluster N is higher at night than during the day. Comparable work in North American migrants has only been performed in one species of swallows, so extension of examination for Cluster N in other migratory birds is needed. In addition, it is unclear if Cluster N activation is lateralized and the full extent of its boundaries in the forebrain have yet to be described. We used sensory-driven gene expression based on ZENK and the Swainson's thrush, a night-migratory North American songbird, to fill these knowledge gaps. We found elevated levels of gene expression in night- vs. day-active thrushes and no evidence for lateralization in this region. We further examined the anatomical extent of neural activation in the forebrain using 3D reconstruction topology. Our findings demonstrate that Swainson's thrushes possess an extensive bilateral night-activated Cluster N region in the forebrain similar to other European avian species, suggesting that Cluster N is highly conserved in nocturnal migrants.

Adaptive evolution and loss of a putative magnetoreceptor in passerines.

Migratory birds possess remarkable accuracy in orientation and navigation, which involves various compass systems including the magnetic compass. Identifying the primary magnetosensor remains a fundamental open question. Cryptochromes (Cry) have been shown to be magnetically sensitive, and Cry4a from a migratory songbird seems to show enhanced magnetic sensitivity in vitro compared to Cry4a from resident species. We investigate Cry and their potential involvement in magnetoreception in a phylogenetic framework, integrating molecular evolutionary analyses with protein dynamics modelling. Our analysis is based on 363 bird genomes and identifies different selection regimes in passerines. We show that Cry4a is characterized by strong positive selection and high variability, typical characteristics of sensor proteins. We identify key sites that are likely to have facilitated the evolution of an optimized sensory protein for night-time orientation in songbirds. Additionally, we show that Cry4 was lost in hummingbirds, parrots and Tyranni (Suboscines), and thus identified a gene deletion, which might facilitate testing the function of Cry4a in birds. In contrast, the other avian Cry (Cry1 and Cry2) were highly conserved across all species, indicating basal, non-sensory functions. Our results support a specialization or functional differentiation of Cry4 in songbirds which could be magnetosensation.

Expression patterns of heat-shock genes during stopover and the trade-off between refueling and stress response in a passerine migrant.

Migrating birds are often exposed to variable environments and face a multitude of stress exposures along their long-distance flights. During stopover refueling, migratory birds must balance the need to accumulate energy reserves to continue their migration with the need to respond to environmental and physiological stressors. We examined the gene expression patterns of different Heat Shock Proteins (HSPs) in migrating birds during stopover at different body condition states (lean vs. fat), to provide some first insights on the role of HSPs in bird migration and explore the concept of a trade-off between refueling and stress response. Our results showed upregulation of HSP expression at release that could be associated with muscle growth and increased cholesterol and lipid synthesis needed for birds to fuel their upcoming migration. On the other hand, during capture, upregulation of HSP5 could be attributed to physiological recovery from the non-stop endurance flight when crossing the Sahara Desert-Mediterranean Sea ecological barrier. All birds significantly increased their fuel loads up to 48% of lean body mass and we provide evidence for muscle rebuilding during stopover as flight muscle mass increased by 10%, highlighting the fact that stopover sites can play a major role in the physiological recovery of migrants.

Climate change drives migratory range shift via individual plasticity in shearwaters.

How individual animals respond to climate change is key to whether populations will persist or go extinct. Yet, few studies investigate how changes in individual behavior underpin these population-level phenomena. Shifts in the distributions of migratory animals can occur through adaptation in migratory behaviors, but there is little understanding of how selection and plasticity contribute to population range shift. Here, we use long-term geolocator tracking of Balearic shearwaters (Puffinus mauretanicus) to investigate how year-to-year changes in individual birds' migrations underpin a range shift in the post-breeding migration. We demonstrate a northward shift in the post-breeding range and show that this is brought about by individual plasticity in migratory destination, with individuals migrating further north in response to changes in sea-surface temperature. Furthermore, we find that when individuals migrate further, they return faster, perhaps minimizing delays in return to the breeding area. Birds apparently judge the increased distance that they will need to migrate via memory of the migration route, suggesting that spatial cognitive mechanisms may contribute to this plasticity and the resulting range shift. Our study exemplifies the role that individual behavior plays in populations' responses to environmental change and highlights some of the behavioral mechanisms that might be key to understanding and predicting species persistence in response to climate change.

Toward understanding the endocrine regulation of diverse facultative migration strategies.

Migration is an important event in the annual cycle of many animals that facilitates the use of resources that vary across space and time. It can occur with regular and predictable timing, as in obligate migration, or with much greater flexibility, as in facultative migration. Most research aimed at understanding the endocrine mechanisms regulating the transition to a migratory stage has focused on obligate migration, whereas less is known about facultative forms of migration. One challenge for research into the endocrine regulation of facultative migration is that facultative migrations encompass a diverse array of migratory movements. Here, we present a framework to describe and conceptualize variation in facultative migrations that focuses on conditions at departure. Within the context of this framework, we review potential endocrine mechanisms involved in the initiation of facultative migrations in vertebrates. We first focus on glucocorticoids, which have been the subject of most research on the topic. We then examine other potential hormones and neurohormones that have received less attention, but are exciting candidates to consider. We conclude by highlighting areas where future research is particularly needed.

Migratory birds are able to choose the appropriate migratory direction under dim yellow narrowband light.

Currently, it is generally assumed that migratory birds are oriented in the appropriate migratory direction under UV, blue and green light (short-wavelength) and are unable to use their magnetic compass in total darkness and under yellow and red light (long-wavelength). However, it has also been suggested that the magnetic compass has two sensitivity peaks: in the short and long wavelengths, but with different intensities. In this project, we aimed to study the orientation of long-distance migrants, pied flycatchers (Ficedula hypoleuca), under different narrowband light conditions during autumn and spring migrations. The birds were tested in the natural magnetic field (NMF) and a changed magnetic field (CMF) rotated counterclockwise by 120° under dim green (autumn) and yellow (spring and autumn) light, which are on the 'threshold' between the short-wavelength and long-wavelength light. We showed that pied flycatchers (i) were completely disoriented under green light both in the NMF and CMF but (ii) showed the migratory direction in the NMF and the appropriate response to CMF under yellow light. Our data contradict the results of previous experiments under narrowband green and yellow light and raise doubts about the existence of only short-wavelength magnetoreception. The parameters of natural light change dramatically in spectral composition and intensity after local sunset, and the avian magnetic compass should be adapted to function properly under such constantly changing light conditions.

Birds of a feather flock together: a dataset for Clock and Adcyap1 genes from migration genetics studies.

Birds in seasonal habitats rely on intricate strategies for optimal timing of migrations. This is governed by environmental cues, including photoperiod. Genetic factors affecting intrinsic timekeeping mechanisms, such as circadian clock genes, have been explored, yielding inconsistent findings with potential lineage-dependency. To clarify this evidence, a systematic review and phylogenetic reanalysis was done. This descriptor outlines the methodology for sourcing, screening, and processing relevant literature and data. PRISMA guidelines were followed, ultimately including 66 studies, with 34 focusing on candidate genes at the genotype-phenotype interface. Studies were clustered using bibliographic coupling and citation network analysis, alongside scientometric analyses by publication year and location. Data was retrieved for allele data from databases, article supplements, and direct author communications. The dataset, version 1.0.2, encompasses data from 52 species, with 46 species for the Clock gene and 43 for the Adcyap1 gene. This dataset, featuring data from over 8000 birds, constitutes the most extensive cross-species collection for these candidate genes, used in studies investigating gene polymorphisms and seasonal bird migration.

Space weather disrupts nocturnal bird migration.

Space weather, including solar storms, can impact Earth by disturbing the geomagnetic field. Despite the known dependence of birds and other animals on geomagnetic cues for successful seasonal migrations, the potential effects of space weather on organisms that use Earth's magnetic field for navigation have received little study. We tested whether space weather geomagnetic disturbances are associated with disruptions to bird migration at a macroecological scale. We leveraged long-term radar data to characterize the nightly migration dynamics of the nocturnally migrating North American avifauna over 22 y. We then used concurrent magnetometer data to develop a local magnetic disturbance index associated with each radar station (ΔBmax), facilitating spatiotemporally explicit analyses of the relationship between migration and geomagnetic disturbance. After controlling for effects of atmospheric weather and spatiotemporal patterns, we found a 9 to 17% decrease in migration intensity in both spring and fall during severe space weather events. During fall migration, we also found evidence for decreases in effort flying against the wind, which may represent a depression of active navigation such that birds drift more with the wind during geomagnetic disturbances. Effort flying against the wind in the fall was most reduced under both overcast conditions and high geomagnetic disturbance, suggesting that a combination of obscured celestial cues and magnetic disturbance may disrupt navigation. Collectively, our results provide evidence for community-wide avifaunal responses to geomagnetic disturbances driven by space weather during nocturnal migration.

The cost of movement: assessing energy expenditure in a long-distant ectothermic migrant under climate change.

Migration is an energetically taxing phenomenon as animals move across vast, heterogeneous landscapes where the cost of transport is impacted by permissible ambient conditions. In this study, we assessed the energetic demands of long-distance migration in a multigenerational ectothermic migrant, the monarch butterfly (Danaus plexippus). We tested the hypotheses that temperature-dependent physiological processes reduce energy reserves faster during migration than previously estimated, and that increasing climatic temperatures resulting from the climate crisis will intensify baseline daily energy expenditure. First, we reared monarchs under laboratory conditions to assess energy and mass conversion from fifth instar to adult stages, as a baseline for migratory adult mass and ontogenetic shifts in metabolic rate from larvae to adult. Then, using historical tag-recapture data, we estimated the movement propensity and migratory pace of autumn migrants using computer simulations and subsequently calculated energy expenditure. Finally, we estimated the energy use of monarchs based on these tag-recapture data and used this information to estimate daily energy expenditure over a 57 year period. We found support for our two hypotheses, noting that incorporating standard metabolic rate into estimates of migratory energy expenditure shows higher energy demand and that daily energy expenditure has been gradually increasing over time since 1961. Our study shows the deleterious energetic consequences under current climate change trajectories and highlights the importance of incorporating energetic estimates for understanding migration by small, ectothermic migrants.

Migratory swans individually adjust their autumn migration and winter range to a warming climate.

In response to climate warming, migratory animals can alter their migration so that different events in the annual cycle are better aligned in space and time with suitable environmental conditions. Although such responses have been studied extensively during spring migration and the breeding season, much less is known about the influence of temperature on movements throughout autumn migration and how those movements result in a winter range and shifts therein. We use multi-year GPS tracking data to quantify how daily autumn movement and annual winter distance from the breeding grounds are related to temperature in the Western Palearctic Bewick's swan, a long-lived migratory waterbird whose winter range has shifted more than 350 km closer to the breeding grounds since 1970 due to individuals increasingly 'short-stopping' their autumn migration. We show that the migratory movement of swans is driven by lower temperatures throughout the autumn season, with individuals during late autumn moving only substantially when temperatures drop below freezing. As a result, there is large flexibility in their annual winter distance as a response to winter temperature. On average, individuals overwinter 118 km closer to the breeding grounds per 1°C increase in mean December-January temperature. Given the observed temperature increase in the Bewick's swan winter range during the last decades, our results imply that the observed range shift is for a substantial part driven by individual responses to a warming climate. We thus present an example of individual flexibility towards climatic conditions driving the range shift of a migratory species. Our study adds to the understanding of the processes that shape autumn migration decisions, winter ranges and shifts therein, which is crucial to be able to predict how climate change may impact these processes in the future.

Gravisensation and modulation of gravitactic responses by other sensory cues in the monarch butterfly (Danaus plexippus).

Using the monarch butterfly (Danaus plexippus), we studied how animals can use cues from multiple sensory modalities for deriving directional information from their environment to display oriented movement. Our work focused on determining how monarchs use gravity as a cue for oriented movement and determined how cues from other sensory modalities, cues that by themselves also produce oriented movement (visual and magnetic directional cues), might modulate gravisensation. In two tests of gravisensation (movement in a vertical tube; righting behavior), we found that monarchs display negative gravitaxis only (movement opposite to the direction of gravity). Negative gravitaxis can be modulated by either visual (light) or magnetic field cues (inclination angle) that provide directional information. The modulation of gravity-mediated responses, however, depends on the relationship between cues when presented during trials, such as when cues are in accord or in conflict. For example, when light cues that elicit positive phototaxis conflicted with negative gravitaxis (light from below the monarch), monarch gravisensation was unaffected by directional light cues. We also found that the antennae play a role in gravity-mediated movement (righting), as, with antennae removed, monarch movement behavior was no longer the same as when the antennae were intact. Our results demonstrate that monarchs can use and integrate multiple, multimodal cues for oriented movement, but that the use of such cues can be hierarchical (that is, one cue dominant for movement), and the hierarchy of cues, and the responses towards them when found together, depends on the physical relationships between cues during movement.

Stopovers Serve Physiological Recovery in Migratory Songbirds.

AbstractMigrating birds perform extreme endurance exercise when flying. This shifts the balance between the production of reactive oxygen species and the antioxidant defense system toward the former, potentially generating oxidative damages. In between migratory flights, birds make stopovers, where besides accumulating fuel (mainly fats), they are assumed to rest and recover from the strenuous flight. We performed a series of studies on both temporarily caged (northern wheatears) and free-flying (northern wheatears and European robins) migrants to investigate whether migrants recover during stopover by decreasing the amount of oxidative lipid damage (malondialdehyde [MDA]) and/or increasing the total nonenzymatic antioxidant capacity (AOX). In caged wheatears, MDA decreased within a single day. These birds were able to simultaneously accumulate considerable amounts of fuel. Also, in the free-flying wheatears, there was a decrease in MDA during stopover; however, this process seemed incompatible with refueling. The reason for this difference could relate to constraints in the wild that are absent in caged birds, such as food limitation/composition and locomotor activity. In the robins, there was a near significant decrease in MDA concentration in relation to how long the birds were already at stopover, suggesting that this species also physiologically recovers during stopover. AOX did not change during stopover in either of the wheatear studies. For the robins, however, uric acid-corrected AOX declined during stopover. Our results show that during stopover, migrating birds rapidly reduce oxidative lipid damage, thereby likely recovering their physiological state. In addition to the commonly accepted function of refueling, stopovers thus probably serve physiological recovery.

Manipulation of photoperiod induces fat storage, but not fat mobilization in the migratory songbird, Dumetella carolinensis (Gray Catbird).

The annual cycle of migratory birds requires significant phenotypic remodeling. We sought to induce the migratory phenotype in Gray Catbirds by exposing them to a short-day light cycle. While adipose storage was stimulated, exceeding that typically seen in wild birds, other aspects of the migratory phenotype were unchanged. Of particular interest, the rate of lipid export from excised adipose tissue was nearly halved. This is in contrast to wild migratory birds in which lipid export rates are increased. These data suggest that exposure to an altered light cycle only activated the lipid storage program while inhibiting the lipid transport program. The factors governing lipid mobilization and transport remain to be elucidated.

Migratory songbirds exhibit seasonal modulation of the oxygen cascade.

Migratory flight requires birds to maintain intensive aerobic exercise for many hours or days. Maintaining O2 supply to flight muscles is therefore important during migration, especially since migratory songbirds have been documented flying at altitudes greater than 5000 m above sea level, where O2 is limited. Whether songbirds exhibit seasonal plasticity of the O2 cascade to maintain O2 uptake and transport during migratory flight is not well understood. We investigated changes in the hypoxic ventilatory response, haematology and pectoralis (flight) muscle phenotype of 6 songbird species from 3 families during migratory and non-migratory conditions. Songbirds were captured during southbound migration in southern Ontario, Canada. Half of the birds were assessed during migration, and the rest were transitioned onto a winter photoperiod to induce a non-migratory phenotype and measured. All species exhibited seasonal plasticity at various stages along the O2 cascade, but not all species exhibited the same responses. Songbirds tended to be more hypoxia tolerant during migration, withstanding 5 kPa O2 and breathed more effectively through slower, deeper breaths. Warblers had a stronger haemoglobin-O2 affinity during autumn migration (decrease of ∼4.7 Torr), while the opposite was observed in thrushes (increase of ∼2.6 Torr). In the flight muscle there was an ∼1.2-fold increase in the abundance of muscle fibres with smaller fibre transverse areas during autumn migration, but no changes in capillary:fibre ratio. These adjustments would enhance O2 uptake and transport to the flight muscle. Our findings demonstrate that in the O2 cascade there is no ideal migratory phenotype for all songbirds.

Rising to the Challenge: Mounting an Acute Phase Immune Response Has No Long-Term Negative Effects on Captive Sparrow Migratory Body Composition or Migratory Restlessness.

Migratory animals may trade-off between investing energy in immune defense versus investing in energy reserves needed for seasonal migration. However, these trade-offs are often masked by other sources of variation and may not be detected through observational field studies of free-living animals. Moreover, observational studies can rarely distinguish the costs of pathogenic infection from those of mounting an immune response. To disentangle such effects, we conducted an immune challenge experiment. We captured song sparrows (Melospiza melodia) and white-throated sparrows (Zonotrichia albicollis) in autumn migratory condition, challenged the sparrows with non-infectious antigens that induce an acute-phase immune response, then monitored body composition and migratory restlessness behavior. For both species, body mass was higher the day after exposure to keyhole limpet hemocyanin (KLH) compared to controls. White-throated sparrows, but not song sparrows, increased lean mass 1 week after exposure to lipopolysaccharide (LPS), suggesting that effects of immune upregulation on body composition may be long-lasting and specific to certain combinations of hosts and antigens. White-throated sparrows exposed to KLH increased nocturnal migratory restlessness (Zugunruhe) for the week following exposure. These findings suggest that short-term activation of the acute immune response does not constrain migratory physiology in these songbirds.

Genetic Control of Avian Migration: Insights from Studies in Latitudinal Passerine Migrants.

Twice-a-year, large-scale movement of billions of birds across latitudinal gradients is one of the most fascinating behavioral phenomena seen among animals. These seasonal voyages in autumn southwards and in spring northwards occur within a discrete time window and, as part of an overall annual itinerary, involve close interaction of the endogenous rhythm at several levels with prevailing photoperiod and temperature. The overall success of seasonal migrations thus depends on their close coupling with the other annual sub-cycles, namely those of the breeding, post-breeding recovery, molt and non-migratory periods. There are striking alterations in the daily behavior and physiology with the onset and end of the migratory period, as shown by the phase inversions in behavioral (a diurnal passerine bird becomes nocturnal and flies at night) and neural activities. Interestingly, there are also differences in the behavior, physiology and regulatory strategies between autumn and spring (vernal) migrations. Concurrent molecular changes occur in regulatory (brain) and metabolic (liver, flight muscle) tissues, as shown in the expression of genes particularly associated with 24 h timekeeping, fat accumulation and the overall metabolism. Here, we present insights into the genetic basis of migratory behavior based on studies using both candidate and global gene expression approaches in passerine migrants, with special reference to Palearctic-Indian migratory blackheaded and redheaded buntings.

Metabolic constraints and individual variation shape the trade-off between physiological recovery and anti-predator responses in adult sockeye salmon.

Metabolic scope represents the aerobic energy budget available to an organism to perform non-maintenance activities (e.g., escape a predator, recover from a fisheries interaction, compete for a mate). Conflicting energetic requirements can give rise to ecologically relevant metabolic trade-offs when energy budgeting is constrained. The objective of this study was to investigate how aerobic energy is utilized when individual sockeye salmon (Oncorhynchus nerka) are exposed to multiple acute stressors. To indirectly assess metabolic changes in free-swimming individuals, salmon were implanted with heart rate biologgers. The animals were then exercised to exhaustion or briefly handled as a control, and allowed to recover from this stressor for 48 h. During the first 2 h of the recovery period, individual salmon were exposed to 90 ml of conspecific alarm cues or water as a control. Heart rate was recorded throughout the recovery period. Recovery effort and time was higher in exercised fish, relative to control fish, whereas exposure to an alarm cue had no effect on either of these metrics. Individual routine heart rate was negatively correlated with recovery time and effort. Together, these findings suggest that metabolic energy allocation towards exercise recovery (i.e., an acute stressor; handling, chase, etc.) trumps anti-predator responses in salmon, although individual variation may mediate this effect at the population level.