Warming temperatures drive at least half of the magnitude of long-term trait changes in European birds.

SignificanceClimate change is impacting wild populations, but its relative importance compared to other causes of change is still unclear. Many studies assume that changes in traits primarily reflect effects of climate change, but this assumption is rarely tested. We show that in European birds global warming was likely the single most important contributor to temporal trends in laying date, body condition, and offspring number. However, nontemperature factors were also important and acted in the same direction, implying that attributing temporal trends solely to rising temperatures overestimates the impact of climate warming. Differences among species in the amount of trait change were predominantly determined by these nontemperature effects, suggesting that species differences are not due to variation in sensitivity to temperature.

Effect of 2020-21 and 2021-22 Highly Pathogenic Avian Influenza H5 Epidemics on Wild Birds, the Netherlands.

The number of highly pathogenic avian influenza (HPAI) H5-related infections and deaths of wild birds in Europe was high during October 1, 2020-September 30, 2022. To quantify deaths among wild species groups with known susceptibility for HPAI H5 during those epidemics, we collected and recorded mortality data of wild birds in the Netherlands. HPAI virus infection was reported in 51 bird species. The species with the highest numbers of reported dead and infected birds varied per epidemic year; in 2020-21, they were within the Anatidae family, in particular barnacle geese (Branta leucopsis) and in 2021-22, they were within the sea bird group, particularly Sandwich terns (Thalasseus sandvicensis) and northern gannet (Morus bassanus). Because of the difficulty of anticipating and modeling the future trends of HPAI among wild birds, we recommend monitoring live and dead wild birds as a tool for surveillance of the changing dynamics of HPAI.

Revisiting Perdeck's massive avian migration experiments debunks alternative social interpretations.

Whether avian migrants can adapt to their changing world depends on the relative importance of genetic and environmental variation for the timing and direction of migration. In the classic series of field experiments on avian migration, A. C. Perdeck discovered that translocated juveniles failed to reach goal areas, whereas translocated adults performed 'true-goal navigation'. His translocations of > 14 000 common starlings (Sturnus vulgaris) suggested that genetic mechanisms guide juveniles into a population-specific direction, i.e. 'vector navigation'. However, alternative explanations involving social learning after release in juveniles could not be excluded. By adding historical data from translocation sites, data that was unavailable in Perdeck's days, and by integrated analyses including the original data, we could not explain juvenile migrations from possible social information upon release. Despite their highly social behaviour, our findings are consistent with the idea that juvenile starlings follow inherited information and independently reach their winter quarters. Similar to more solitarily migrating songbirds, starlings would require genetic change to adjust the migration route in response to global change.

Earlier springs increase goose breeding propensity and nesting success at Arctic but not at temperate latitudes.

Intermittent breeding is an important tactic in long-lived species that trade off survival and reproduction to maximize lifetime reproductive success. When breeding conditions are unfavourable, individuals are expected to skip reproduction to ensure their own survival. Breeding propensity (i.e. the probability for a mature female to breed in a given year) is an essential parameter in determining reproductive output and population dynamics, but is not often studied in birds because it is difficult to obtain unbiased estimates. Breeding conditions are especially variable at high latitudes, potentially resulting in a large effect on breeding propensity of Arctic-breeding migratory birds, such as geese. With a novel approach, we used GPS-tracking data to determine nest locations, breeding propensity and nesting success of barnacle geese, and studied how these varied with breeding latitude and timing of arrival on the breeding grounds relative to local onset of spring. Onset of spring at the breeding grounds was a better predictor of breeding propensity and nesting success than relative timing of arrival. At Arctic latitudes (>66° N), breeding propensity decreased from 0.89 (95% CI: 0.65-0.97) in early springs to 0.22 (95% CI: 0.06-0.55) in late springs, while at temperate latitudes, it varied between 0.75 (95% CI: 0.38-0.93) and 0.89 (95% CI: 0.41-0.99) regardless of spring phenology. Nesting success followed a similar pattern and was lower in later springs at Arctic latitudes, but not at temperate latitudes. In early springs, a larger proportion of geese started breeding despite arriving late relative to the onset of spring, possibly because the early spring enabled them to use local resources to fuel egg laying and incubation. While earlier springs due to climate warming are considered to have mostly negative repercussions on reproductive success through phenological mismatches, our results suggest that these effects may partly be offset by higher breeding propensity and nesting success.

Year-round activity levels reveal diurnal foraging constraints in the annual cycle of migratory and non-migratory barnacle geese.

Performing migratory journeys comes with energetic costs, which have to be compensated within the annual cycle. An assessment of how and when such compensation occurs is ideally done by comparing full annual cycles of migratory and non-migratory individuals of the same species, which is rarely achieved. We studied free-living migratory and resident barnacle geese belonging to the same flyway (metapopulation), and investigated when differences in foraging activity occur, and when foraging extends beyond available daylight, indicating a diurnal foraging constraint in these usually diurnal animals. We compared foraging activity of migratory (N = 94) and resident (N = 30) geese throughout the annual cycle using GPS-transmitters and 3D-accelerometers, and corroborated this with data on seasonal variation in body condition. Migratory geese were more active than residents during most of the year, amounting to a difference of over 370 h over an entire annual cycle. Activity differences were largest during the periods that comprised preparation for spring and autumn migration. Lengthening days during spring facilitated increased activity, which coincided with an increase in body condition. Both migratory and resident geese were active at night during winter, but migratory geese were also active at night before autumn migration, resulting in a period of night-time activity that was 6 weeks longer than in resident geese. Our results indicate that, at least in geese, seasonal migration requires longer daily activity not only during migration but throughout most of the annual cycle, with migrants being more frequently forced to extend foraging activity into the night.

Postnatal growth rate varies with latitude in range-expanding geese: The role of plasticity and day length.

The postnatal growth period is a crucial life stage, with potential lifelong effects on an animal's fitness. How fast animals grow depends on their life-history strategy and rearing environment, and interspecific comparisons generally show higher growth rates at higher latitudes. However, to elucidate the mechanisms behind this gradient in growth rate, intraspecific comparisons are needed. Recently, barnacle geese expanded their Arctic breeding range from the Russian Barents Sea coast southwards, and now also breed along the Baltic and North Sea coasts. Baltic breeders shortened their migration, while barnacle geese breeding along the North Sea stopped migrating entirely. We collected cross-sectional data on gosling tarsus length, head length and body mass, and constructed population-specific growth curves to compare growth rates among three populations (Barents Sea, Baltic Sea and North Sea) spanning 17° in latitude. Growth rate was faster at higher latitudes, and the gradient resembled the latitudinal gradient previously observed in an interspecific comparison of precocial species. Differences in day length among the three breeding regions could largely explain the observed differences in growth rate. In the Baltic, and especially in the Arctic population, growth rate was slower later in the season, most likely because of the stronger seasonal decline in food quality. Our results suggest that differences in postnatal growth rate between the Arctic and temperate populations are mainly a plastic response to local environmental conditions. This plasticity can increase the individuals' ability to cope with annual variation in local conditions, but can also increase the potential to re-distribute and adapt to new breeding environments.

Individual variability and versatility in an eco-evolutionary model of avian migration.

Seasonal migration is a complex and variable behaviour with the potential to promote reproductive isolation. In Eurasian blackcaps (Sylvia atricapilla), a migratory divide in central Europe separating populations with southwest (SW) and southeast (SE) autumn routes may facilitate isolation, and individuals using new wintering areas in Britain show divergence from Mediterranean winterers. We tracked 100 blackcaps in the wild to characterize these strategies. Blackcaps to the west and east of the divide used predominantly SW and SE directions, respectively, but close to the contact zone many individuals took intermediate (S) routes. At 14.0° E, we documented a sharp transition from SW to SE migratory directions across only 27 (10-86) km, implying a strong selection gradient across the divide. Blackcaps wintering in Britain took northwesterly migration routes from continental European breeding grounds. They originated from a surprisingly extensive area, spanning 2000 km of the breeding range. British winterers bred in sympatry with SW-bound migrants but arrived 9.8 days earlier on the breeding grounds, suggesting some potential for assortative mating by timing. Overall, our data reveal complex variation in songbird migration and suggest that selection can maintain variation in migration direction across short distances while enabling the spread of a novel strategy across a wide range.

Ontogenetic niche shifts as a driver of seasonal migration.

Ontogenetic niche shifts have helped to understand population dynamics. Here we show that ontogenetic niche shifts also offer an explanation, complementary to traditional concepts, as to why certain species show seasonal migration. We describe how demographic processes (survival, reproduction and migration) and associated ecological requirements of species may change with ontogenetic stage (juvenile, adult) and across the migratory range (breeding, non-breeding). We apply this concept to widely different species (dark-bellied brent geese (Branta b. bernicla), humpback whales (Megaptera novaeangliae) and migratory Pacific salmon (Oncorhynchus gorbuscha) to check the generality of this hypothesis. Consistent with the idea that ontogenetic niche shifts are an important driver of seasonal migration, we find that growth and survival of juvenile life stages profit most from ecological conditions that are specific to breeding areas. We suggest that matrix population modelling techniques are promising to detect the importance of the ontogenetic niche shifts in maintaining migratory strategies. As a proof of concept, we applied a first analysis to resident, partial migratory and fully migratory populations of barnacle geese (Branta leucopsis). We argue that recognition of the costs and benefits of migration, and how these vary with life stages, is important to understand and conserve migration under global environmental change.

Detection of West Nile virus in a common whitethroat (Curruca communis) and Culex mosquitoes in the Netherlands, 2020.

On 22 August, a common whitethroat in the Netherlands tested positive for West Nile virus lineage 2. The same bird had tested negative in spring. Subsequent testing of Culex mosquitoes collected in August and early September in the same location generated two of 44 positive mosquito pools, providing first evidence for enzootic transmission in the Netherlands. Sequences generated from the positive mosquito pools clustered with sequences that originate from Germany, Austria and the Czech Republic.

Climate warming may affect the optimal timing of reproduction for migratory geese differently in the low and high Arctic.

Rapid climate warming is driving organisms to advance timing of reproduction with earlier springs, but the rate of advancement shows large variation, even among populations of the same species. In this study, we investigated how the rate of advancement in timing of reproduction with a warming climate varies for barnacle goose (Branta leucopsis) populations breeding at different latitudes in the Arctic. We hypothesized that populations breeding further North are generally more time constrained and, therefore, produce clutches earlier relative to the onset of spring than southern populations. Therefore, with increasing temperatures and a progressive relief of time constraint, we expected latitudinal differences to decrease. For the years 2000-2016, we determined the onset of spring from snow cover data derived from satellite images, and compiled data on egg laying date and reproductive performance in one low-Arctic and two high-Arctic sites. As expected, high-Arctic geese laid their eggs earlier relative to snowmelt than low-Arctic geese. Contrary to expectations, advancement in laying dates was similar in high- and low-Arctic colonies, at a rate of 27% of the advance in date of snowmelt. Although advancement of egg laying did not fully compensate for the advancement of snowmelt, geese laying eggs at intermediate dates in the low Arctic were the most successful breeders. In the high Arctic, however, early nesting geese were the most successful breeders, suggesting that high-Arctic geese have not advanced their laying dates sufficiently to earlier springs. This indicates that high-Arctic geese especially are vulnerable to negative effects of climate warming.

Climate change leads to differential shifts in the timing of annual cycle stages in a migratory bird.

Shifts in reproductive phenology due to climate change have been well documented in many species but how, within the same species, other annual cycle stages (e.g. moult, migration) shift relative to the timing of breeding has rarely been studied. When stages shift at different rates, the interval between stages may change resulting in overlaps, and as each stage is energetically demanding, these overlaps may have negative fitness consequences. We used long-term data of a population of European pied flycatchers (Ficedula hypoleuca) to investigate phenological shifts in three annual cycle stages: spring migration (arrival dates), breeding (egg-laying and hatching dates) and the onset of postbreeding moult. We found different advancements in the timing of breeding compared with moult (moult advances faster) and no advancement in arrival dates. To understand these differential shifts, we explored which temperatures best explain the year-to-year variation in the timing of these stages, and show that they respond differently to temperature increases in the Netherlands, causing the intervals between arrival and breeding and between breeding and moult to decrease. Next, we tested the fitness consequences of these shortened intervals. We found no effect on clutch size, but the probability of a fledged chick to recruit increased with a shorter arrival-breeding interval (earlier breeding). Finally, mark-recapture analyses did not detect an effect of shortened intervals on adult survival. Our results suggest that the advancement of breeding allows more time for fledgling development, increasing their probability to recruit. This may incur costs to other parts of the annual cycle, but, despite the shorter intervals, there was no effect on adult survival. Our results show that to fully understand the consequences of climate change, it is necessary to look carefully at different annual cycle stages, especially for organisms with complex cycles, such as migratory birds.

Local amplification of highly pathogenic avian influenza H5N8 viruses in wild birds in the Netherlands, 2016 to 2017.

IntroductionHighly pathogenic avian influenza (HPAI) viruses of subtype H5N8 were re-introduced into the Netherlands by late 2016, after detections in south-east Asia and Russia. This second H5N8 wave resulted in a large number of outbreaks in poultry farms and the deaths of large numbers of wild birds in multiple European countries. Methods: Here we report on the detection of HPAI H5N8 virus in 57 wild birds of 12 species sampled during active (32/5,167) and passive (25/36) surveillance activities, i.e. in healthy and dead animals respectively, in the Netherlands between 8 November 2016 and 31 March 2017. Moreover, we further investigate the experimental approach of wild bird serology as a contributing tool in HPAI outbreak investigations. Results: In contrast to the first H5N8 wave, local virus amplification with associated wild bird mortality has occurred in the Netherlands in 2016/17, with evidence for occasional gene exchange with low pathogenic avian influenza (LPAI) viruses. Discussion: These apparent differences between outbreaks and the continuing detections of HPAI viruses in Europe are a cause of concern. With the current circulation of zoonotic HPAI and LPAI virus strains in Asia, increased understanding of the drivers responsible for the global spread of Asian poultry viruses via wild birds is needed.

Deaths among Wild Birds during Highly Pathogenic Avian Influenza A(H5N8) Virus Outbreak, the Netherlands.

During autumn-winter 2016-2017, highly pathogenic avian influenza A(H5N8) viruses caused mass die-offs among wild birds in the Netherlands. Among the ≈13,600 birds reported dead, most were tufted ducks (Aythya fuligula) and Eurasian wigeons (Anas penelope). Recurrence of avian influenza outbreaks might alter wild bird population dynamics.

Widespread activity of multiple lineages of Usutu virus, western Europe, 2016.

In the summer of 2016, Belgium, France, Germany and the Netherlands reported widespread Usutu virus (USUV) activity based on live and dead bird surveillance. The causative USUV strains represented four lineages, of which two putative novel lineages were most likely recently introduced into Germany and spread to other western European countries. The spatial extent of the outbreak area corresponded with R0 values > 1. The occurrence of the outbreak, the largest USUV epizootic registered so far in Europe, allowed us to gain insight in how a recently introduced arbovirus with potential public health implications can spread and become a resident pathogen in a naïve environment. Understanding the ecological and epidemiological factors that drive the emergence or re-emergence of USUV is critical to develop and implement timely surveillance strategies for adequate preventive and control measures. Public health authorities, blood transfusion services and clinicians in countries where USUV was detected should be aware of the risk of possible USUV infection in humans, including in patients with unexplained encephalitis or other neurological impairments, especially during late summer when mosquito densities peak.

Lack of virological and serological evidence for continued circulation of highly pathogenic avian influenza H5N8 virus in wild birds in the Netherlands, 14 November 2014 to 31 January 2016.

In 2014, H5N8 clade 2.3.4.4 highly pathogenic avian influenza (HPAI) viruses of the A/Goose/Guangdong/1/1996 lineage emerged in poultry and wild birds in Asia, Europe and North America. Here, wild birds were extensively investigated in the Netherlands for HPAI H5N8 virus (real-time polymerase chain reaction targeting the matrix and H5 gene) and antibody detection (haemagglutination inhibition and virus neutralisation assays) before, during and after the first virus detection in Europe in late 2014. Between 21 February 2015 and 31 January 2016, 7,337 bird samples were tested for the virus. One HPAI H5N8 virus-infected Eurasian wigeon (Anas penelope) sampled on 25 February 2015 was detected. Serological assays were performed on 1,443 samples, including 149 collected between 2007 and 2013, 945 between 14 November 2014 and 13 May 2015, and 349 between 1 September and 31 December 2015. Antibodies specific for HPAI H5 clade 2.3.4.4 were absent in wild bird sera obtained before 2014 and present in sera collected during and after the HPAI H5N8 emergence in Europe, with antibody incidence declining after the 2014/15 winter. Our results indicate that the HPAI H5N8 virus has not continued to circulate extensively in wild bird populations since the 2014/15 winter and that independent maintenance of the virus in these populations appears unlikely.

Forecasting spring from afar? Timing of migration and predictability of phenology along different migration routes of an avian herbivore.

Herbivorous birds are hypothesized to migrate in spring along a seasonal gradient of plant profitability towards their breeding grounds (green wave hypothesis). For Arctic breeding species in particular, following highly profitable food is important, so that they can replenish resources along the way and arrive in optimal body condition to start breeding early. We compared the timing of migratory movements of Arctic breeding geese on different flyways to examine whether flyways differed in the predictability of spring conditions at stopovers and whether this was reflected in the degree to which birds were following the green wave. Barnacle geese (Branta leucopsis) were tracked with solar GPS/ARGOS PTTs from their wintering grounds to breeding sites in Greenland (N = 7), Svalbard (N = 21) and the Barents Sea (N = 12). The numerous stopover sites of all birds were combined into a set of 16 general stopover regions. The predictability of climatic conditions along the flyways was calculated as the correlation and slope between onsets of spring at consecutive stopovers. These values differed between sites, mainly because of the presence or absence of ecological barriers. Goose arrival at stopovers was more closely tied to the local onset of spring when predictability was higher and when geese attempted breeding that year. All birds arrived at early stopovers after the onset of spring and arrived at the breeding grounds before the onset of spring, thus overtaking the green wave. This is in accordance with patterns expected for capital breeders: first, they must come into condition; at intermediate stopovers, arrival with the food quality peak is important to stay in condition, and at the breeding grounds, early arrival is favoured so that hatching of young can coincide with the peak of food quality. Our results suggest that a chain of correlations between climatic conditions at subsequent stopovers enables geese to closely track the green wave. However, the birds' precision of migratory timing seems uninfluenced by ecological barriers, indicating partly fixed migration schedules. These might become non-optimal due to climate warming and preclude accurate timing of long-distance migrants in the future.

Temporal dynamics of bird community composition: an analysis of baseline conditions from long-term data.

Numerous anthropogenic activities threaten the biodiversity found on earth. Because all ecological communities constantly experience temporal turnover due to natural processes, it is important to distinguish between change due to anthropogenic impact and the underlying natural rate of change. In this study, we used data sets on breeding bird communities that covered at least 20 consecutive years, from a variety of terrestrial ecosystems, to address two main questions. (1) How fast does the composition of bird communities change over time, and can we identify a baseline of natural change that distinguishes primeval systems from systems experiencing varying degrees of human impact? (2) How do patterns of temporal variation in composition vary among bird communities in ecosystems with different anthropogenic impacts? Time lag analysis (TLA) showed a pattern of increasing rate of temporal compositional change from large-scale primeval systems to disturbed and protected systems to distinctly successional systems. TLA slopes of <0.04 were typical for breeding bird communities with natural turnover, while communities subjected to anthropogenic impact were characterised by TLA slopes of >0.04. Most of the temporal variability of breeding bird communities was explained by slow changes occurring over decades, regardless of the intensity of human impact. In most of the time series, medium- and short-wave periodicity was not detected, with the exception of breeding bird communities subjected to periodic pulses (e.g. caterpillar outbreaks causing food resource peaks).

Sentinel chicken surveillance reveals previously undetected circulation of West Nile virus in the Netherlands.

AbstractWest Nile virus (WNV) was first detected in the Netherlands in 2020, with circulation observed in birds, mosquitoes, and humans in two geographical areas. Usutu virus (USUV) has been circulating in the Netherlands since 2016. Following the detection of WNV in the Netherlands, we investigated the possible use of petting zoos as urban sentinel sites to examine the extent of WNV and USUV circulation around the two WNV outbreak locations.Chickens at petting zoos and in backyards were sampled within a 15-kilometer radius of the confirmed WNV circulation areas at three timepoints over one year (2021-2022). Sera were analyzed using a protein microarray for binding antibodies to orthoflavivirus NS1 antigens and reactive samples were confirmed through micro-focus reduction neutralization tests (mFRNT). Furthermore, mosquitoes at sampling locations were collected to assess their blood feeding behaviour.This serosurvey detected the circulation of USUV and WNV in petting zoo and backyard chickens in 2021, both within and outside the 2020 outbreak areas. The WNV circulation was not detected by other existing surveillance schemes in mosquitoes, wild birds, horses and humans. In addition, the results show rapid decay of USUV antibodies in approximately 20 weeks. Our findings support the utility and the added value of petting zoo chickens as sentinels for monitoring USUV and WNV circulation compared to other available methods. Seroconversions observed in petting zoos and backyard chickens living in or near densely populated urban areas further highlighted potential public health risks that went undetected.

Ixodes ricinus as potential vector for Usutu virus.

Usutu virus (USUV) is an emerging flavivirus that is maintained in an enzootic cycle with mosquitoes as vectors and birds as amplifying hosts. In Europe, the virus has caused mass mortality of wild birds, mainly among Common Blackbird (Turdus merula) populations. While mosquitoes are the primary vectors for USUV, Common Blackbirds and other avian species are exposed to other arthropod ectoparasites, such as ticks. It is unknown, however, if ticks can maintain and transmit USUV. We addressed this question using in vitro and in vivo experiments and field collected data. USUV replicated in IRE/CTVM19 Ixodes ricinus tick cells and in injected ticks. Moreover, I. ricinus nymphs acquired the virus via artificial membrane blood-feeding and maintained the virus for at least 70 days. Transstadial transmission of USUV from nymphs to adults was confirmed in 4.9% of the ticks. USUV disseminated from the midgut to the haemocoel, and was transmitted via the saliva of the tick during artificial membrane blood-feeding. We further explored the role of ticks by monitoring USUV in questing ticks and in ticks feeding on wild birds in the Netherlands between 2016 and 2019. In total, 622 wild birds and the Ixodes ticks they carried were tested for USUV RNA. Of these birds, 48 (7.7%) carried USUV-positive ticks. The presence of negative-sense USUV RNA in ticks, as confirmed via small RNA-sequencing, showed active virus replication. In contrast, we did not detect USUV in 15,381 questing ticks collected in 2017 and 2019. We conclude that I. ricinus can be infected with USUV and can transstadially and horizontally transmit USUV. However, in comparison to mosquito-borne transmission, the role of I. ricinus ticks in the epidemiology of USUV is expected to be minor.

Structural genomic variation and migratory behavior in a wild songbird.

Structural variants (SVs) are a major source of genetic variation; and descriptions in natural populations and connections with phenotypic traits are beginning to accumulate in the literature. We integrated advances in genomic sequencing and animal tracking to begin filling this knowledge gap in the Eurasian blackcap. Specifically, we (a) characterized the genome-wide distribution, frequency, and overall fitness effects of SVs using haplotype-resolved assemblies for 79 birds, and (b) used these SVs to study the genetics of seasonal migration. We detected >15 K SVs. Many SVs overlapped repetitive regions and exhibited evidence of purifying selection suggesting they have overall deleterious effects on fitness. We used estimates of genomic differentiation to identify SVs exhibiting evidence of selection in blackcaps with different migratory strategies. Insertions and deletions dominated the SVs we identified and were associated with genes that are either directly (e.g., regulatory motifs that maintain circadian rhythms) or indirectly (e.g., through immune response) related to migration. We also broke migration down into individual traits (direction, distance, and timing) using existing tracking data and tested if genetic variation at the SVs we identified could account for phenotypic variation at these traits. This was only the case for 1 trait-direction-and 1 specific SV (a deletion on chromosome 27) accounted for much of this variation. Our results highlight the evolutionary importance of SVs in natural populations and provide insight into the genetic basis of seasonal migration.