Molecular changes and physiological responses involved in migratory bird fuel management and stopover decisions.

Migratory birds undertake long journeys across continents to reach breeding habitats with abundant resources. These migrations are essential for their survival and are shaped by a complex interplay of physiological adaptations, behavioral cues, and gene expression patterns. Central to migration are stopovers, critical resting points where birds replenish energy stores before continuing their journey. In this study, we integrate physiological measurements, behavioral observations, and molecular data from temporarily caged migrating Garden Warblers (Sylvia borin) to gain insights into their stopover strategies and physiological adaptations after crossing the extended ecological barrier formed by the Sahara Desert and the Mediterranean Sea. Depleted individuals, marked by low body mass and flight muscle mass, showcased remarkable plasticity in recovering and rapidly rebuilding energy stores within a short 5-day stopover. Flight muscle mass increased during this period, highlighting a dynamic trade-off between muscle rebuilding and refuelling. Notably, birds prioritizing muscle rebuilding exhibited a trade-off with the downregulation of genes related to lipid transport and metabolism and at the same time showing evidence of skeletal muscle angiogenesis. Early arrivals were more motivated to depart and exhibited higher levels of physiological stress. Our study highlights the importance of understanding the adaptive responses of birds to changing environmental conditions along their migration routes.

First detection and a new avian host of the tick Ixodes ventalloi Gil Collado, 1936, in Slovakia.

This study describes the first detection of Ixodes ventalloi in Slovakia. Two engorged females of I. ventalloi were collected from Dunnocks (Prunella modularis) captured in eastern Slovakia. The identification of females was based on morphological and molecular 16S rRNA gene features. Phylogenetic analysis revealed a classification of the females into distinct genogroups. Moreover, comparative morphological analysis highlighted variations between the two females, particularly in the curvature of the auriculae, the shape of coxa I, and the internal spur. These findings suggest the potential for varied phenotypes of I. ventalloi correlated with their genogroups. Nonetheless, I. ventalloi population establishment within Slovakia necessitates further investigation through flagging or drag sampling.

Chasing and surfing seasonal waves: Avian migration through the US tracks land surface phenology in fall, but not spring.

Climate change is altering the timing of seasonal events for many taxa. There is limited understanding of how northward/southward songbird migration follows or is limited by the latitudinal progression of seasonal transitions. Consistent environmental conditions that migrating birds encounter across latitudes likely represent or correlate with important resources or limiting factors for migration. We tested whether migratory passage-observed via radar-consistently tracked land surface variables and phenophases across latitudes in the US Central Flyway in both spring and fall. The daily temperatures, precipitation and vegetation greenness occurring on 10%, 50% and 90% cumulative passage dates changed substantially with latitude, indicating that most migrants experienced rapidly changing conditions as they headed north or south. Temperature did not limit the progression of migration in either season. Peak spring migration in the southern US occurred nearly 40 days after the spring green wave, the northward progression of vegetation growth, but nearly caught up to green-up at 48° N. Spring migration phenology may have evolved to prioritize earlier arrival for breeding. Across all latitudes, peak fall migration coincided with the same land surface phenophase, an interval of 26 days prior to dormancy onset. Migrants may rely on phenological events in vegetation during fall stopovers. Considering that (a) migratory passage tracked fall land surface phenology across latitudes at a continental scale, (b) previous studies at local scales have demonstrated the importance of fruit during fall migratory stopover and (c) fruiting phenology in North America is occurring later over time while fall migration is advancing, the potential for mismatch between fall fruiting and bird migration phenology urgently needs further investigation.

Predicting resilience of migratory birds to environmental change.

The pace and scale of environmental change represent major challenges to many organisms. Animals that move long distances, such as migratory birds, are especially vulnerable to change since they need chains of intact habitat along their migratory routes. Estimating the resilience of such species to environmental changes assists in targeting conservation efforts. We developed a migration modeling framework to predict past (1960s), present (2010s), and future (2060s) optimal migration strategies across five shorebird species (Scolopacidae) within the East Asian-Australasian Flyway, which has seen major habitat deterioration and loss over the last century, and compared these predictions to empirical tracks from the present. Our model captured the migration strategies of the five species and identified the changes in migrations needed to respond to habitat deterioration and climate change. Notably, the larger species, with single or few major stopover sites, need to establish new migration routes and strategies, while smaller species can buffer habitat loss by redistributing their stopover areas to novel or less-used sites. Comparing model predictions with empirical tracks also indicates that larger species with the stronger need for adaptations continue to migrate closer to the optimal routes of the past, before habitat deterioration accelerated. Our study not only quantifies the vulnerability of species in the face of global change but also explicitly reveals the extent of adaptations required to sustain their migrations. This modeling framework provides a tool for conservation planning that can accommodate the future needs of migratory species.

Controlled expression of avian pre-migratory fattening influences indices of innate immunity.

While immunity is frequently dampened when birds engage in strenuous migratory flights, whether and how immunity changes during the rapid accumulation of energy stores in preparation for migration remains largely unknown. Here we induced pre-migratory fattening through controlled changes of daylight in common quails (Coturnix coturnix) and regularly assessed changes in three markers of constitutive innate immunity (leukocyte coping capacity or LCC, hemagglutination and hemolysis titres) and measures of body composition (lean and fat mass). All the three markers showed similar changes over the pre-migratory fattening process. LCC responses, hemagglutination titres, and hemolysis titres, were on average higher in the mid-fattening phase compared to the peak-fattening phase, when values were similar to those observed prior the start of pre-migratory fattening. At mid-fattening, we found that the birds that showed a larger accumulation of fat mass (as % of body mass) had lower LCC peak responses and hemolysis titres. Reversibly, at mid-fattening, we also found that the birds that kept a higher proportion of lean mass (as % of body mass) had the highest LCC peaks. Our results indicate that migratory birds undergo changes in immune indices (over 8 weeks) as they accumulate energy stores for migration and propose that this could be due to competing or trade-off processes between metabolic remodelling and innate immune system function.

A multi-sensor array for detecting and analyzing nocturnal avian migration.

Avian migration has fascinated humans for centuries. Insights into the lives of migrant birds are often elusive; however, recent, standalone technological innovations have revolutionized our understanding of this complex biological phenomenon. A future challenge for following these highly mobile animals is the necessity of bringing multiple technologies together to capture a more complete understanding of their movements. Here, we designed a proof-of-concept multi-sensor array consisting of two weather surveillance radars (WSRs), one local and one regional, an autonomous moon-watching sensor capable of detecting birds flying in front of the moon, and an autonomous recording unit (ARU) capable of recording avian nocturnal flight calls. We deployed this array at a field site in central Oklahoma on select nights in March, April, and May of 2021 and integrated data from this array with wind data corresponding to this site to examine the influence of wind on the movements of spring migrants aloft across these spring nights. We found that regional avian migration intensity is statistically significantly negatively correlated with wind velocity, in line with previous research. Furthermore, we found evidence suggesting that when faced with strong, southerly winds, migrants take advantage of these conditions by adjusting their flight direction by drifting. Importantly, we found that most of the migration intensities detected by the sensors were intercorrelated, except when this correlation could not be ascertained because we lacked the sample size to do so. This study demonstrates the potential for multi-sensor arrays to reveal the detailed ways in which avian migrants move in response to changing atmospheric conditions while in flight.

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.

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.

Assemblages of Plasmodium and Related Parasites in Birds with Different Migration Statuses.

Migratory birds spend several months in their breeding grounds in sympatry with local resident birds and relatively shorter periods of time at stopover sites. During migration, parasites may be transmitted between migratory and resident birds. However, to what extent they share these parasites remains unclear. In this study, we compared the assemblages of haemosporidian parasites in migratory, resident, and passing birds, as well as the correlations between parasite assemblages and host phylogeny. Compared with passing birds, migratory birds were more likely to share parasites with resident birds. Shared lineages showed significantly higher prevalence rates than other lineages, indicating that common parasites are more likely to spill over from the current host to other birds. For shared lineages, the prevalence was significantly higher in resident birds than in migratory birds, suggesting that migratory birds pick up parasites at their breeding ground. Among the shared lineages, almost two-thirds presented no phylogenetic signal in their prevalence, indicating that parasite transmission among host species is weakly or not correlated with host phylogeny. Moreover, similarities between parasite assemblages are not correlated with either migration status or the phylogeny of hosts. Our results show that the prevalence, rather than host phylogeny, plays a central role in parasite transmission between migratory and resident birds in breeding grounds.

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.

Phenological trends in the pre- and post-breeding migration of long-distance migratory birds.

Phenological mismatch is often cited as a putative driver of population declines in long-distance migratory birds. The mechanisms and cues utilized to advance breeding ground arrival will impact the adaptability of species to further warming. Furthermore, timing of post-breeding migration potentially faces diverging selective pressures, with earlier onset of tropical dry seasons favouring migration advancement, while longer growing seasons in temperate areas could facilitate delayed departures. Despite this, few studies exist of migration phenology on the non-breeding grounds or on post-breeding passage. Here, we use first arrival and last departure dates of 20 species of trans-Saharan migratory birds from tropical non-breeding grounds (The Gambia), between 1964 and 2019. Additionally, we use first arrival and last departure dates, as well as median arrival and departure dates, at an entry/departure site to/from Europe (Gibraltar), between 1991 and 2018. We assess phenological trends in pre- and post-breeding migration, as well as individual species' durations of stay in breeding and non-breeding areas. Furthermore, we assess the extent to which inter-annual variation in these timings may be explained by meteorological and ecological variables. We find significant advances in pre-breeding migration at both locations, while post-breeding migration is delayed. At Gibraltar, these trends do not differ between first/last and median dates of migration. The combination of these trends suggests substantial changes in the temporal usage of the two continents by migratory birds. Duration of stay (of species, not individuals) within Europe increased by 16 days, on average, over the 27-year monitoring period. By contrast, duration of species' stays on the non-breeding range declined by 63 days, on average, over the 56-year monitoring period. Taken together these changes suggest substantial, previously unreported alterations to annual routines in Afro-Palaearctic migrants.

Ghrelin, not corticosterone, is associated with transitioning of phenotypic states in a migratory Galliform.

In both captive and free-living birds, the emergence of the migratory phenotype is signalled by rapid and marked increases in food intake and fuelling, as well as changes in amount of nocturnality or migratory restlessness. The metabolic hormone corticosterone and, as more recently suggested, the gut-derived hormone ghrelin have been suggested to play a role in mediating such phenomenal phenotypic flexibility given that they both regulate fuel metabolism and locomotion across vertebrate taxa. Here, using the Common quail (Coturnix coturnix) as our study species, we induced autumn migration followed by a non-migratory wintering phase through controlled changes in daylight. We thus compared plasma corticosterone and ghrelin concentrations between the two sampling phases and assessed whether these hormones might reflect the migratory state. While we found no differences in plasma corticosterone between the two sampling phases and no link of this hormone with changes in body mass, levels of food intake or migratory restlessness, the migratory birds had substantially higher levels of plasma ghrelin relative to the non-migratory birds. Furthermore, while ghrelin did not correlate with the gain in body mass over the entire pre-migratory fuelling phase (over an average of nine weeks preceding blood sampling), plasma ghrelin did positively correlate with the gain in body mass observed during the final fattening stages (over an average of three weeks preceding blood sampling). Again, variation in plasma ghrelin also reflected the amount of body mass depleted over both the long- and short-time frame as birds returned to their non-migratory baseline - lower levels of plasma ghrelin consistently correlated with larger losses in body mass. Thus, while our data do not highlight a role of the hormone corticosterone in sustaining pre-migratory fattening as shown in other bird species, they do add evidence for a potential role of ghrelin in mediating migratory behaviour and further suggest that this hormone might be important in regulating the transitioning of migratory states, possibly by promoting fuel mobilisation and usage.

Migration stopover ecology of Cinnamon Teal in western North America.

Identifying migration routes and fall stopover sites of Cinnamon Teal (Spatula cyanoptera septentrionalium) can provide a spatial guide to management and conservation efforts, and address vulnerabilities in wetland networks that support migratory waterbirds. Using high spatiotemporal resolution GPS-GSM transmitters, we analyzed 61 fall migration tracks across western North America during our three-year study (2017-2019). We marked Cinnamon Teal primarily during spring/summer in important breeding and molting regions across seven states (California, Oregon, Washington, Idaho, Utah, Colorado, and Nevada). We assessed fall migration routes and timing, detected 186 fall stopover sites, and identified specific North American ecoregions where sites were located. We classified underlying land cover for each stopover site and measured habitat selection for 12 land cover types within each ecoregion. Cinnamon Teal selected a variety of flooded habitats including natural, riparian, tidal, and managed wetlands; wet agriculture (including irrigation ditches, flooded fields, and stock ponds); wastewater sites; and golf and urban ponds. Wet agriculture was the most used habitat type (29.8% of stopover locations), and over 72% of stopover locations were on private land. Relatively scarce habitats such as wastewater ponds, tidal marsh, and golf and urban ponds were highly selected in specific ecoregions. In contrast, dry non-habitat across all ecoregions, and dry agriculture in the Cold Deserts and Mediterranean California ecoregions, was consistently avoided. Resources used by Cinnamon Teal often reflected wetland availability across the west and emphasize their adaptability to dynamic resource conditions in arid landscapes. Our results provide much needed information on spatial and temporal resource use by Cinnamon Teal during migration and indicate important wetland habitats for migrating waterfowl in the western United States.

Migration and season explain tick prevalence in Brazilian birds.

Neotropical birds are mostly parasitized by immature ticks and act as reservoir hosts of tick-borne pathogens of medical and veterinary interest. Hence, determining the factors that enable ticks to encounter these highly mobile hosts and increase the potential for tick dispersal throughout migratory flyways are important for understanding tick-borne disease transmission. We used 9682 individual birds from 572 species surveyed across Brazil and Bayesian models to disentangle possible avian host traits and climatic drivers of infestation probabilities, accounting for avian host phylogenetic relationships and spatiotemporal factors that may influence tick prevalence. Our models revealed that the probability of an individual bird being infested with tick larvae and nymphs was lower in partial migrant hosts and during the wet season. Notably, infestation probability increased in areas with a higher proportion of partial migrant birds. Other avian ecological traits known to influence tick prevalence (foraging habitat and body mass) and environmental condition that might constrain tick abundance (annual precipitation and minimum temperature) did not explain infestation probability. Our findings suggest that migratory flyways harbouring a greater abundance of migrant bird hosts also harbour a higher prevalence of immature ticks with potential to enhance the local transmission of tick-borne pathogens and spread across regions.

Controlled expression of the migratory phenotype affects oxidative status in birds.

High caloric intake can increase production of reactive oxygen and nitrogen species. We examined whether the emergence of the migratory phenotype, primarily signalled by increased food intake and fuelling, is accompanied by changes in oxidative status. We induced autumn migration followed by a non-migratory wintering phase in common quails (Coturnix coturnix). We compared three markers of oxidative status - oxidative damage to lipids expressed as thiobarbituric acid reactive substances (TBARS); superoxide dismutase (SOD); and glutathione peroxidase (GPx) - between birds sampled during the migratory and non-migratory phase. We found that the emergence of the migratory phenotype was associated with: (i) higher levels of TBARS in the liver; (ii) lower levels of SOD in red blood cells and, marginally, in the liver; (iii) higher levels of GPx in the pectoral muscle; and (iv) sex-specific changes in red blood cells and liver. We found no link between food intake and variation in markers of oxidative status in any of the tissues examined, despite food intake being higher in the migratory birds. However, the increase in body mass was positively correlated with muscle GPx activity as birds entered the pre-migratory fattening phase, while the amount of decrease in body mass was negatively correlated with muscle GPx as birds transitioned to the non-migratory phase. Such correlations were absent in red blood cells and liver. Our work suggests that during the emergence of the migratory phenotype, birds might strategically displace oxidative costs on the liver in order to safeguard the pectoral muscles, which have a fundamental role in successfully completing the migratory flight.

Avian Malaria and Related Parasites from Resident and Migratory Birds in the Brazilian Atlantic Forest, with Description of a New Haemoproteus Species.

Determining the prevalence and local transmission dynamics of parasitic organisms are necessary to understand the ability of parasites to persist in host populations and disperse across regions, yet local transmission dynamics, diversity, and distribution of haemosporidian parasites remain poorly understood. We studied the prevalence, diversity, and distributions of avian haemosporidian parasites of the genera Plasmodium, Haemoproteus, and Leucocytozoon among resident and migratory birds in Serra do Mar, Brazil. Using 399 blood samples from 66 Atlantic Forest bird species, we determined the prevalence and molecular diversity of these pathogens across avian host species and described a new species of Haemoproteus. Our molecular and morphological study also revealed that migratory species were infected more than residents. However, vector infective stages (gametocytes) of Leucocytozoon spp., the most prevalent parasites found in the most abundant migrating host species in Serra do Mar (Elaenia albiceps), were not seen in blood films of local birds suggesting that this long-distance Austral migrant can disperse Leucocytozoon parasite lineages from Patagonia to the Atlantic Forest, but lineage sharing among resident species and local transmission cannot occur in this part of Brazil. Our study demonstrates that migratory species may harbor a higher diversity and prevalence of parasites than resident species, but transportation of some parasites by migratory hosts may not always affect local transmission.

Data on the de novo transcriptome assembly for the migratory bird, the Common quail (Coturnix coturnix).

The Common or European quail (Coturnix coturnix) is a Galliform bird of ecological importance for research in the field of animal migration. The Common quail is also a game bird, thus, of great interest for recreational activities and conservation management. Here, we generated a high quality de novo transcriptome for the Common quail for which no reference genome is to date publicly available. The transcriptome was obtained from a population of Common quail originated from captive founders raised under laboratory conditions. Paired-end RNA-Sequencing reads were obtained from extracted total RNA of brain tissue punches (preoptic-hypothalamic region) of 23 quails, which yielded to 5.5-11.2 million reads per individual bird for a total of 236 million reads. After assembly optimization, we used a stringent filtering analysis pipeline to remove redundant and low confidence transcripts. The final transcriptome consisted of 22,293 transcripts of which 21,551 (97%) were provided with annotation data. Our data offers a high quality pipeline for compiling transcriptomes of complex non-genomic species. Our data also provide a robust reference for gene expression studies in this species or other related Galliform species, including the Japanese quail.

Host movement and time of year influence tick parasitism in Pantanal birds.

Ticks are among the best studied parasitic groups as they spread important pathogens of medical and veterinary importance worldwide. Migratory birds can play an important role in transporting ticks infected with pathogens across wide geographic regions. It is therefore important to understand which factors promote tick parasitism rates across their avian hosts and the associated potential for disease spread. Here, we identified the host attributes of infestation probability of ticks from the genus Amblyomma in 955 birds from Pantanal, Brazil. Infestation rates exhibited considerable variation across the 129 avian species surveyed and were explained by both host ecological traits and evolutionary history. The probability of an individual bird being infested with immature ticks (larvae and/or nymphs) was higher across resident bird species that forage at ground level and during the wet season. Bird species that feed on vertebrates were less likely to be infested by ticks. Other ecological traits known to promote tick exposure (age, body mass, social behavior, and sex) did not predict infestation probability. Our findings demonstrate that tick occurrence in Pantanal birds is determined by avian host attributes, but tick occurrence throughout the year constrains exposure to host-seeking ticks. Moreover, the ecology of the avian host might prevent the potential spread of tick-borne diseases outside Pantanal as migratory hosts are likely less infested by ticks.

Metabolic reduction after long-duration flight is not related to fat-free mass loss or flight duration in a migratory passerine.

Migratory birds catabolize large quantities of protein during long flights, resulting in dramatic reductions in organ and muscle mass. One of the many hypotheses to explain this phenomenon is that decrease in lean mass is associated with reduced resting metabolism, saving energy after flight during refueling. However, the relationship between lean body mass and resting metabolic rate remains unclear. Furthermore, the coupling of lean mass with resting metabolic rate and with peak metabolic rate before and after long-duration flight have not previously been explored. We flew migratory yellow-rumped warblers (Setophaga coronata) in a wind tunnel under one of two humidity regimes to manipulate the rate of lean mass loss in flight, decoupling flight duration from total lean mass loss. Before and after long-duration flights, we measured resting and peak metabolism, and also measured fat mass and lean body mass using quantitative magnetic resonance. Flight duration ranged from 28 min to 600 min, and birds flying under dehydrating conditions lost more fat-free mass than those flying under humid conditions. After flight, there was a 14% reduction in resting metabolism but no change in peak metabolism. Interestingly, the reduction in resting metabolism was unrelated to flight duration or to change in fat-free body mass, indicating that protein metabolism in flight is unlikely to have evolved as an energy-saving measure to aid stopover refueling, but metabolic reduction itself is likely to be beneficial to migratory birds arriving in novel habitats.

Haemosporidian parasites of resident and wintering migratory birds in The Bahamas.

In temperate regions, some avian haemosporidian parasites have evolved seasonal transmission strategies, with chronic infections relapsing during spring and transmission peaking during the hosts' breeding season. Because lineages with seasonal transmission strategies are unlikely to produce gametocytes in winter, we predicted that (1) resident birds living within wintering areas of Neotropical migrants would unlikely be infected with North American parasite lineages; and (2) if infected, wintering migratory birds would be more likely to harbor Plasmodium spp. rather than Parahaemoproteus spp. or Haemoproteus spp. parasites in their bloodstreams, as only Plasmodium produces life stages, other than gametocytes, that infect red blood cells. To test these predictions, we used molecular detection and microscopy to compare the diversity and prevalence of haemosporidian parasites among year-round residents and wintering migratory birds during February 2016, on three islands of The Bahamas archipelago, i.e., Andros, Grand Bahama, and Great Abaco. Infection prevalence was low and comparable between migratory (15/111) and resident (15/129) individuals, and it did not differ significantly among islands. Out of the 12 lineages detected infecting migratory birds, five were transmitted in North America; four lineages could have been transmitted during breeding, wintering, or migration; and three lineages were likely transmitted in The Bahamas. Resident birds mostly carried lineages endemic to the Caribbean region. All North American-transmitted parasite lineages detected among migratory birds were Plasmodium spp. Our findings suggest that haemosporidian parasites of migrants shift resource allocation seasonally, minimizing the production of gametocytes during winter, with low risk of infection spillover to resident birds.