The effects of cities on quail (Coturnix coturnix) migration: a disturbing story of population connectivity, health, and ecography.

The increasing impact of human activities on ecosystems is provoking a profound and dangerous effect, particularly in wildlife. Examining the historical migration patterns of quail (Coturnix coturnix) offers a compelling case study to demonstrate the repercussions of human actions on biodiversity. Urbanization trends, where people gravitate toward mega-urban areas, amplify this effect. The proliferation of artificial urban ecosystems extends its influence across every biome, as human reliance on infrastructure and food sources alters ecological dynamics extensively. We examine European quail migrations pre- and post-World War II and in the present day. Our study concentrates on the Italian peninsula, investigating the historical and contemporary recovery of ringed quail populations. To comprehend changes in quail migration, we utilize trajectory analysis, open statistical data, and linear generalized models. We found that while human population and economic growth have shown a linear increase, quail recovery rates exhibit a U-shaped trajectory, and cereal and legume production displays an inverse U-shaped pattern. Generalized linear models have unveiled the significant influence of several key factors-time periods, cereal and legume production, and human demographics-on quail recovery rates. These factors closely correlate with the levels of urbanization observed across these timeframes. These insights underscore the profound impact of expanding human populations and the rise of mega-urbanization on ecosystem dynamics and services. As our planet becomes more urbanized, the pressure on ecosystems intensifies, highlighting the urgent need for concerted efforts directed toward conserving and revitalizing ecosystem integrity. Simultaneously, manage the needs and demands of burgeoning mega-urban areas. Achieving this balance is pivotal to ensuring sustainable coexistence between urban improvement and the preservation of our natural environment.

Avian Haemosporidians Infecting Short- and Long-Distance Migratory Old World Flycatcher Species and the Variation in Parasitaemia After Endurance Flights.

PURPOSE: Avian haemosporidians are widespread parasites, occurring in many bird families and causing pathologies ranging from rather benign infections to highly virulent diseases. The state of knowledge about lineage-specific intensities of haemosporidian infection (i.e., parasitaemia) is mainly based on infection experiments conducted under laboratory conditions. The levels and range of parasitaemia in natural host-parasite associations as well as their influencing factor remain largely unexplored. METHODS: Thus, we explored the parasitaemia of four songbird species (i.e., European Robins, Black and Common Redstarts and Whinchats) during migration by screening individuals upon landing on an insular passage site after extensive endurance flights to (1) describe their natural host-parasite associations, (2) quantify parasitaemia and (3) explore potential host- and parasite-related factors influencing parasitaemia. RESULTS: We found 68% of Whinchats to be infected with haemosporidians, which is more frequent than any other of the studied host species (30-34%). Furthermore, we confirmed that parasitaemia of Haemoproteus infections was higher than average Plasmodium infections. Median parasitaemia levels were rather low (parasite cells in 0.01% of hosts' red blood cells) and varied largely among the different parasite lineages. However, we found four individuals hosting infections with parasitaemia higher than typical chronic infections. CONCLUSIONS: Based on the known transmission areas of the respective lineages, we argue that these higher intensity infections might be relapses of consisting infections rather than acute phases of recent primary infections.

Modelling the timing of migration of a partial migrant bird using ringing and observation data: a case study with the Song Thrush in Italy.

BACKGROUND: The study of the timing of migration is fundamental to the understanding of the ecology of many bird species and their response to climate change, and it has important conservation and management implications e.g., for assessing the hunting seasons according to the EU Directive 2009/147/EC (Birds Directive). METHODS: We developed a new method for the analysis of ringing data (both first capture and re-encounters) and citizen science observations, to assess the timing of pre- and post-nuptial migration of birds. This method was tested on the Song Thrush Turdus philomelos, using i) the Bird Ringing Database hosted by the ISPRA Italian Ringing Centre from the whole Italian peninsula, the three closest large islands (Sicily, Sardinia and Corsica), and Canton Ticino (Switzerland) and ii) the eBird data for the same study area. RESULTS: The results from both datasets consistently showed that pre-nuptial migration starts during the first 10-day period of January (Jan 1) in some central and southern areas of the Italian peninsula, in central Sicily, southern Sardinia, and Corsica. The onset of migration occurs on Jan 2 in the rest of central and southern Italy, Sicily and Sardinia, and western Liguria, while it starts later in the north-eastern Alps, up to Mar 3. The end of post-nuptial migration is more synchronous, occurring on Nov 1 across most of Italy, slightly earlier (Oct 3) in northern Italy and later (Nov 2) in Sicily. The uncertainty of the estimated dates was < 2 days in most cases. CONCLUSION: This method represents a novel and valuable tool for the analyses of the timing of migration using ringing and citizen science data and provides an important contribution to the Key Concepts Document of the EU Birds Directive, where migration timings are considered and used to define the hunting period of birds.

Reconstructing migratory network nodes to improve environmental management and conservation decisions: A case study of the common quail Coturnix coturnix as a biosensor.

Public health risks are related to environmental management practices, and are essential to the understanding of ecosystem dynamics. The expansion of urbanized areas affects migratory bird networks and can impact the population sizes of migratory species and, in parallel, increase the risk of diseases carried by migratory species spreading into urban areas. Taking the European population of the common quail as a case study, we reconstructed its migratory network between Europe and the Maghreb using quail recoveries from the Italian Bird Ringing Scheme. We showed that soils at the central European migratory node have been degraded through urbanization and reforestation, decreasing the number of successful migrations over this area. Conceptual models incorporating the One Health approach, natural and social capital, landscape infrastructure, and ecosystem services could explain the relationships between climate warming and extensively developed, intensively developed, and urbanized ecosystems. Failed migratory flights of quail over central Europe highlight not only the problems of infrastructure design and their impact on ecosystems services, but also on One Health parameters. The damage to migratory network nodes presents a global threat to biodiversity and can increase the spread of diseases. To address this challenge we propose: i) improvements in land quality; ii) transboundary migration monitoring programmes; and iii) management plans for migratory birds - the overall aim being to optimize infrastructures to improve the quality of human life. Lessons drawn from a better understanding of the migratory networks of quail in relation to different ecosystems provide useful tools to improve infrastructure management and political decision making processes.

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.

Direct and Indirect Role of Migratory Birds in Spreading CCHFV and WNV: A Multidisciplinary Study on Three Stop-Over Islands in Italy.

The annual movements of migratory birds can contribute to the spread of African ticks and tick-borne pathogens of potential public health concern across Europe. The aim of the study was to investigate their role in the possible introduction of African ticks and tick-borne pathogens into European countries during spring migration. A total of 2344 ticks were collected during three spring seasons from 1079 birds captured on three Italian stop-over islands during their northbound migration. Once identified, each tick was tested by RT-PCR for the presence of Crimean-Congo hemorrhagic fever (CCHFV), West Nile (WNV), and Usutu (USUV) viruses. Moreover, carcasses of birds found dead were collected and tested for the possible presence of WNV and USUV. Results confirmed a higher contribution of trans-Saharan migrants compared to intra-Palearctic ones and the prevalence of African tick species in the sample. CCHFV was detected for the second time in Italy in a Hyalomma rufipes, and WNV was found in two ticks of the same genus, all carried by trans-Saharan birds. WNV lineage 1 was also found in the organs of a Garden warbler. These results confirm the role of migratory birds in carrying African ticks, as well as viruses of zoonotic importance, from Africa into Europe.

West Nile and Usutu Virus Introduction via Migratory Birds: A Retrospective Analysis in Italy.

The actual contribution of migratory birds in spreading West Nile (WNV) and Usutu virus (USUV) across Europe and from Africa to old countries is still controversial. In this study, we reported the results of molecular and serological surveys on migrating birds sampled during peaks of spring and autumn migration at 11 Italian sites located along important flyways, from 2012 to 2014. A total of 1335 specimens made of individual or pooled sera, and organs from 275 dead birds were tested for WNV and USUV RNA by real time PCR (RT-PCR). Furthermore, sera were tested by serum neutralization assay for detecting WNV and USUV neutralizing antibodies. Molecular tests detected WNV lineage 2 RNA in a pool made of three Song Thrush (Turdus philomelos) sera sampled in autumn, and lineage 1 in kidneys of six trans-Saharan birds sampled in spring. Neutralizing antibodies against WNV and USUV were found in 5.80% (n = 72; 17 bird species) and 0.32% (n = 4; 4 bird species) of the tested sera, respectively. Our results do not exclude the role of migratory birds as potential spreaders of WNV and USUV from Africa and Central Europe to Mediterranean areas and highlight the importance of a more extensive active surveillance of zoonotic viruses.

Short- and long-distance avian migrants differ in exercise endurance but not aerobic capacity.

BACKGROUND: Migratory birds differ markedly in their migration strategies, particularly those performing short- versus long-distance migrations. In preparation for migration, all birds undergo physiological and morphological modifications including enlargement of fat stores and pectoral muscles to fuel and power their flights, as well as cardiovascular and biochemical adjustments that improve lipid and oxygen delivery and uptake by flight muscles. While the magnitude of these changes varies in relation to migration strategy, the consequence of these variations on aerobic performance is unknown. We tested whether the aerobic performance of four Old-world flycatcher species (Muscicapidae) varied according to migration strategy by comparing minimum resting metabolic rates (RMRmin), exercise-induced maximum metabolic rates (MMR), and exercise endurance times of short-distance and long-distance migratory birds. RESULTS: As expected, RMRmin did not vary between short-distance and long-distance migrants but differed between the species within a migration strategy and between sexes. Unexpectedly, MMR did not vary with migration strategy, but MMR and blood haemoglobin content were positively related among the birds tested. Exercise endurance times differed substantially between migration strategies with long-distance migrants sustaining exercise for > 60% longer than short-distance migrants. Blood haemoglobin content had a significant positive effect on endurance among all birds examined. CONCLUSIONS: The lack of difference in RMRmin and MMR between long- and short-distance migrants during this stage of migration suggests that the attributes favouring the greater aerobic endurance of long-distance migrants did not come at the expense of increased maintenance costs or require greater aerobic capacity.

A deepening understanding of animal culture suggests lessons for conservation.

A key goal of conservation is to protect biodiversity by supporting the long-term persistence of viable, natural populations of wild species. Conservation practice has long been guided by genetic, ecological and demographic indicators of risk. Emerging evidence of animal culture across diverse taxa and its role as a driver of evolutionary diversification, population structure and demographic processes may be essential for augmenting these conventional conservation approaches and decision-making. Animal culture was the focus of a ground-breaking resolution under the Convention on the Conservation of Migratory Species of Wild Animals (CMS), an international treaty operating under the UN Environment Programme. Here, we synthesize existing evidence to demonstrate how social learning and animal culture interact with processes important to conservation management. Specifically, we explore how social learning might influence population viability and be an important resource in response to anthropogenic change, and provide examples of how it can result in phenotypically distinct units with different, socially learnt behavioural strategies. While identifying culture and social learning can be challenging, indirect identification and parsimonious inferences may be informative. Finally, we identify relevant methodologies and provide a framework for viewing behavioural data through a cultural lens which might provide new insights for conservation management.

Comparing population trend estimates of migratory birds from breeding censuses and capture data at a spring migration bottleneck.

Europe has a well-established network of breeding bird monitoring that is used to produce supranational indices of population trends for many species. However, a comparison of breeding bird censuses with other methods may be beneficial to confirm the validity of such indices. The aim of this study was to assess the value of standardized capture data of migratory birds at migration bottlenecks as an indicator of the effective breeding populations. One limitation to this method is that several populations are co-occurring at these bottlenecks and their catchment areas need to be clearly identified to allow extrapolation of population indices. Here, we used standardized trends in capture numbers of 30 species on the island of Ponza, a migration bottleneck in the central Mediterranean, and compared them to population trends estimated in the putative catchment breeding areas between 2005 and 2016. The catchment areas were identified through the analysis of ring recoveries during the breeding season of birds passing through Ponza. Our results show an agreement between the population trends observed on Ponza and those in the breeding areas in 15 out of 30 species. The correlations were strongest in species with a more robust definition of the catchment areas, that is, species with more than 10 recoveries, and for which the recoveries were most likely of breeding birds. The main reason for disagreement between the two indices in the remaining species might be related to different intensity of sampling in different areas. This issue can be solved by further developing monitoring projects in underrepresented countries, as well as by intensifying monitoring through ringing, both in the breeding grounds and at migration bottlenecks. These results show that spring migration monitoring at bottlenecks has the potential to provide a valuable complement and an independent control of breeding bird surveys, allowing raising early warnings of population declines and contributing to their conservation.

Prevalence and genetic diversity of avian haemosporidian parasites in wild bird species of the order Columbiformes.

Diseases can play a role in species decline. Among them, haemosporidian parasites, vector-transmitted protozoan parasites, are known to constitute a risk for different avian species. However, the magnitude of haemosporidian infection in wild columbiform birds, including strongly decreasing European turtle doves, is largely unknown. We examined the prevalence and diversity of haemosporidian parasites Plasmodium, Leucocytozoon and subgenera Haemoproteus and Parahaemoproteus in six species of the order Columbiformes during breeding season and migration by applying nested PCR, one-step multiplex PCR assay and microscopy. We detected infections in 109 of the 259 screened individuals (42%), including 15 distinct haemosporidian mitochondrial cytochrome b lineages, representing five H. (Haemoproteus), two H. (Parahaemoproteus), five Leucocytozoon and three Plasmodium lineages. Five of these lineages have never been described before. We discriminated between single and mixed infections and determined host species-specific prevalence for each parasite genus. Observed differences among sampled host species are discussed with reference to behavioural characteristics, including nesting and migration strategy. Our results support previous suggestions that migratory birds have a higher prevalence and diversity of blood parasites than resident or short-distance migratory species. A phylogenetic reconstruction provided evidence for H. (Haemoproteus) as well as H. (Parahaemoproteus) infections in columbiform birds. Based on microscopic examination, we quantified parasitemia, indicating the probability of negative effects on the host. This study provides a large-scale baseline description of haemosporidian infections of wild birds belonging to the order Columbiformes sampled in the northern hemisphere. The results enable the monitoring of future changes in parasite transmission areas, distribution and diversity associated with global change, posing a potential risk for declining avian species as the European turtle dove.

The genome sequence of the European nightjar, Caprimulgus europaeus (Linnaeus, 1758).

We present a genome assembly from an individual female Caprimulgus europaeus (the European nightjar; Chordata; Aves; Caprimulgiformes; Caprimulgidae). The genome sequence is 1,178 megabases in span. The majority of the assembly (99.33%) is scaffolded into 37 chromosomal pseudomolecules, including the W and Z sex chromosomes.

Recent phenological shifts of migratory birds at a Mediterranean spring stopover site: Species wintering in the Sahel advance passage more than tropical winterers.

Spring migration phenology is shifting towards earlier dates as a response to climate change in many bird species. However, the patterns of change might not be the same for all species, populations, sex and age classes. In particular, patterns of change could differ between species with different ecology. We analyzed 18 years of standardized bird capture data at a spring stopover site on the island of Ponza, Italy, to determine species-specific rates of phenological change for 30 species following the crossing of the Mediterranean Sea. The advancement of spring passage was more pronounced in species wintering in Northern Africa (i.e. short-distance migrants) and in the Sahel zone. Only males from species wintering further South in the forests of central Africa advanced their passage, with no effect on the overall peak date of passage of the species. The migration window on Ponza broadened in many species, suggesting that early migrants within a species are advancing their migration more than late migrants. These data suggest that the cues available to the birds to adjust departure might be changing at different rates depending on wintering location and habitat, or that early migrants of different species might be responding differently to changing conditions along the route. However, more data on departure time from the wintering areas are required to understand the mechanisms underlying such phenological changes.

Evolution of chain migration in an aerial insectivorous bird, the common swift Apus apus.

Spectacular long-distance migration has evolved repeatedly in animals enabling exploration of resources separated in time and space. In birds, these patterns are largely driven by seasonality, cost of migration, and asymmetries in competition leading most often to leapfrog migration, where northern breeding populations winter furthest to the south. Here, we show that the highly aerial common swift Apus apus, spending the nonbreeding period on the wing, instead exhibits a rarely found chain migration pattern, where the most southern breeding populations in Europe migrate to wintering areas furthest to the south in Africa, whereas the northern populations winter to the north. The swifts concentrated in three major areas in sub-Saharan Africa during the nonbreeding period, with substantial overlap of nearby breeding populations. We found that the southern breeding swifts were larger, raised more young, and arrived to the wintering areas with higher seasonal variation in greenness (Normalized Difference Vegetation Index) earlier than the northern breeding swifts. This unusual chain migration pattern in common swifts is largely driven by differential annual timing and we suggest it evolves by prior occupancy and dominance by size in the breeding quarters and by prior occupancy combined with diffuse competition in the winter.

Assessing the role of migratory birds in the introduction of ticks and tick-borne pathogens from African countries: An Italian experience.

The continuous flow of billions of birds between Africa and Europe creates an "ecological bridge" between physically remote areas. Migratory birds fly south from their breeding grounds during late summer/fall and fly back in spring. These movements regulate the spread of internal and external parasites, as well as pathogens of potential public health concern. The aim of the present study was to investigate the possible introduction of exotic tick species and tick-borne pathogens into Europe via migratory birds. At the bird observatory of Ventotene island (Italy), 443 feeding ticks were collected from 249 birds captured and ringed during their northbound migration in spring 2013. Each tick was identified by morphological and molecular methods and then tested for bacterial and viral pathogens: Borrelia burgdorferi s.l., Rickettsia spp., Ehrlichia ruminantium and Coxiella burnetii, Crimean Congo haemorrhagic fever virus (CCHFV) and Flavivirus. Morphological and molecular identification confirmed Hyalomma rufipes as the most abundant species among the collected arthropods (366/443; 82.6%) followed by Hyalomma marginatum (10/433; 2.3%). Rickettsia aeschlimannii was identified in 158 ticks, while one engorged Amblyomma variegatum nymph was infected with Rickettsia africae. The other bacteria were not detected in any specimen. Among viruses, RNA belonging to West Nile virus and other Flavivirus were detected whereas all ticks were negative for CCHFV RNA. These results confirm how migratory birds play a role in carrying Rickettsia-infected ticks, as well as viruses of zoonotic importance, from Africa into Europe. To what extent tick species are capable of establishing a permanent population once introduced in naïve areas, is far from defined and deserve further investigation.

Crimean-Congo Hemorrhagic Fever Virus Genome in Tick from Migratory Bird, Italy.

We detected Crimean-Congo hemorrhagic fever virus in a Hyalomma rufipes nymph collected from a whinchat (Saxicola rubetra) on the island of Ventotene in April 2017. Partial genome sequences suggest the virus originated in Africa. Detection of the genome of this virus in Italy confirms its potential dispersion through migratory birds.

Patterns of Midichloria infection in avian-borne African ticks and their trans-Saharan migratory hosts.

BACKGROUND: Ticks are obligate haematophagous ectoparasites of vertebrates and frequently parasitize avian species that can carry them across continents during their long-distance migrations. Ticks may have detrimental effects on the health state of their avian hosts, which can be either directly caused by blood-draining or mediated by microbial pathogens transmitted during the blood meal. Indeed, ticks host complex microbial communities, including bacterial pathogens and symbionts. Midichloria bacteria (Rickettsiales) are widespread tick endosymbionts that can be transmitted to vertebrate hosts during the tick bite, inducing an antibody response. Their actual role as infectious/pathogenic agents is, however, unclear. METHODS: We screened for Midichloria DNA African ticks and blood samples collected from trans-Saharan migratory songbirds at their arrival in Europe during spring migration. RESULTS: Tick infestation rate was 5.7%, with most ticks belonging to the Hyalomma marginatum species complex. Over 90% of Hyalomma ticks harboured DNA of Midichloria bacteria belonging to the monophylum associated with ticks. Midichloria DNA was detected in 43% of blood samples of avian hosts. Tick-infested adult birds were significantly more likely to test positive to the presence of Midichloria DNA than non-infested adults and second-year individuals, suggesting a long-term persistence of these bacteria within avian hosts. Tick parasitism was associated with a significantly delayed timing of spring migration of avian hosts but had no significant effects on body condition, whereas blood Midichloria DNA presence negatively affected fat deposits of tick-infested avian hosts. CONCLUSIONS: Our results show that ticks effectively transfer Midichloria bacteria to avian hosts, supporting the hypothesis that they are infectious to vertebrates. Bird infection likely enhances the horizontal spread of these bacteria across haematophagous ectoparasite populations. Moreover, we showed that Midichloria and tick parasitism have detrimental non-independent effects on avian host health during migration, highlighting the complexity of interactions involving ticks, their vertebrate hosts, and tick-borne bacteria.

High prevalence of Trichomonas gallinae in wild columbids across western and southern Europe.

BACKGROUND: Avian trichomonosis is known as a widespread disease in columbids and passerines, and recent findings have highlighted the pathogenic character of some lineages found in wild birds. Trichomonosis can affect wild bird populations including endangered species, as has been shown for Mauritian pink pigeons Nesoenas mayeri in Mauritius and suggested for European turtle doves Streptopelia turtur in the UK. However, the disease trichomonosis is caused only by pathogenic lineages of the parasite Trichomonas gallinae. Therefore, understanding the prevalence and distribution of both potentially pathogenic and non-pathogenic T. gallinae lineages in turtle doves and other columbids across Europe is relevant to estimate the potential impact of the disease on a continental scale. RESULTS: We examined 281 samples from four wild columbid species for Trichomonas infection and determined the genetic lineages. The overall prevalence was 74%. There were significant differences between the species (P = 0.007). The highest prevalence was found in stock doves Columba oenas (86%, n = 79) followed by wood pigeons Columba palumbus (70%, n = 61) and turtle doves (67%, n = 65), while three of five collared doves Streptopelia decaocto (60%) were infected. We found seven different lineages, including four lineages present in columbids in the UK, one lineage already described from Spain and three new lineages, one of those found in a single turtle dove migrating through Italy and another one found in a breeding stock dove. Stock doves from Germany and collared doves from Malta were infected with a potentially pathogenic lineage (lineage A/B), which is known to cause lesions and mortality in columbids, raptors and finches. CONCLUSIONS: Generally, turtle doves showed high prevalence of Trichomonas infection. Furthermore, the potentially pathogenic lineage A/B (or genotype B according to previous literature) was found in a recovering stock dove population. Both findings are worrying for these columbid species due to the occasional epidemic character of trichomonosis, which can have severe negative effects on populations.

Candidate genes have sex-specific effects on timing of spring migration and moult speed in a long-distance migratory bird.

The timing of major life-history events, such as migration and moult, is set by endogenous circadian and circannual clocks, that have been well characterized at the molecular level. Conversely, the genetic sources of variation in phenology and in other behavioral traits have been sparsely addressed. It has been proposed that inter-individual variability in the timing of seasonal events may arise from allelic polymorphism at phenological candidate genes involved in the signaling cascade of the endogenous clocks. In this study of a long-distance migratory passerine bird, the willow warbler Phylloscopus trochilus, we investigated whether allelic variation at 5 polymorphic loci of 4 candidate genes (Adcyap1, Clock, Creb1, and Npas2), predicted 2 major components of the annual schedule, namely timing of spring migration across the central Mediterranean sea and moult speed, the latter gauged from ptilochronological analyses of tail feathers moulted in the African winter quarters. We identified a novel Clock gene locus (Clock region 3) showing polyQ polymorphism, which was however not significantly associated with any phenotypic trait. Npas2 allele size predicted male (but not female) spring migration date, with males bearing longer alleles migrating significantly earlier than those bearing shorter alleles. Creb1 allele size significantly predicted male (but not female) moult speed, longer alleles being associated with faster moult. All other genotype-phenotype associations were statistically non-significant. These findings provide new evidence for a role of candidate genes in modulating the phenology of different circannual activities in long-distance migratory birds, and for the occurrence of sex-specific candidate gene effects.