Wild Passerine Research Articles

Metatranscriptomic Comparison of Viromes in Endemic and Introduced Passerines in New Zealand.

New Zealand/Aotearoa has many endemic passerine birds vulnerable to emerging infectious diseases. Yet little is known about viruses in passerines, and in some countries, including New Zealand, the virome of wild passerines has been only scarcely researched. Using metatranscriptomic sequencing we characterised the virome of New Zealand endemic and introduced species of passerine. Accordingly, we identified 34 possible avian viruses from cloacal swabs of 12 endemic and introduced bird species not showing signs of disease. These included a novel siadenovirus, iltovirus, and avastrovirus in the Eurasian blackbird (Turdus merula, an introduced species), song thrush (Turdus philomelos, introduced) and silvereye/tauhou (Zosterops lateralis, introduced), respectively. This is the first time novel viruses from these genera have been identified in New Zealand, likely reflecting prior undersampling. It also represents the first identification of an iltovirus and siadenovirus in blackbirds and thrushes globally. These three viruses were only found in introduced species and may pose a risk to endemic species if they were to jump species boundaries, particularly the iltoviruses and siadenoviruses that have a prior history of disease associations. Further virus study and surveillance are needed in New Zealand avifauna, particularly in Turdus populations and endemic species.

Combining host and vector data informs emergence and potential impact of an Usutu virus outbreak in UK wild birds

Following the first detection in the United Kingdom of Usutu virus (USUV) in wild birds in 2020, we undertook a multidisciplinary investigation that combined screening host and vector populations with interrogation of national citizen science monitoring datasets to assess the potential for population impacts on avian hosts. Pathological findings from six USUV-positive wild passerines were non-specific, highlighting the need for molecular and immunohistochemical examinations to confirm infection. Mosquito surveillance at the index site identified USUV RNA in Culex pipiens s.l. following the outbreak. Although the Eurasian blackbird (Turdus merula) is most frequently impacted by USUV in Europe, national syndromic surveillance failed to detect any increase in occurrence of clinical signs consistent with USUV infection in this species. Furthermore, there was no increase in recoveries of dead blackbirds marked by the national ringing scheme. However, there was regional clustering of blackbird disease incident reports centred near the index site in 2020 and a contemporaneous marked reduction in the frequency with which blackbirds were recorded in gardens in this area, consistent with a hypothesis of disease-mediated population decline. Combining results from multidisciplinary schemes, as we have done, in real-time offers a model for the detection and impact assessment of future disease emergence events.

Male song stability shows cross-year repeatability but does not affect reproductive success in a wild passerine bird.

Predictable behaviour (or 'behavioural stability') might be favoured in certain ecological contexts, for example when representing a quality signal. Costs associated with producing stable phenotypes imply selection should favour plasticity in stability when beneficial. Repeatable among-individual differences in degree of stability are simultaneously expected if individuals differ in ability to pay these costs, or in how they resolve cost-benefit trade-offs. Bird song represents a prime example, where stability may be costly yet beneficial when stable singing is a quality signal favoured by sexual selection. Assuming energetic costs, ecological variation (e.g. in food availability) should result in both within- and among-individual variation in stability. If song stability represents a quality signal, we expect directional selection favouring stable singers. For a 3-year period, we monitored 12 nest box plots of great tits Parus major during breeding. We recorded male songs during simulated territory intrusions, twice during their mate's laying stage and twice during incubation. Each preceding winter, we manipulated food availability. Assuming that stability is costly, we expected food-supplemented males to sing more stable songs. We also expected males to sing more stable songs early in the breeding season (when paternity is not decided) and stable singers to have increased reproductive success. We found strong support for plasticity in stability for two key song characteristics: minimum frequency and phrase length. Males were plastic because they became more stable over the season, contrary to expectations. Food supplementation did not affect body condition but increased stability in minimum frequency. This treatment effect occurred only in 1 year, implying that food supplementation affected stability only in interaction with (unknown) year-specific ecological factors. We found no support for directional, correlational or fluctuating selection on the stability in minimum frequency (i.e. the song trait whose stability exhibited cross-year repeatability): stable singers did not have higher reproductive success. Our findings imply that stability in minimum frequency is not a fitness quality indicator unless males enjoy fitness benefits via pathways not studied here. Future studies should thus address the mechanisms shaping and maintaining individual repeatability of song stability in the wild.

Unravelling the causes and consequences of dispersal syndromes in a wild passerine.

Evidence accumulates that dispersal is correlated with individual behavioural phenotype (dispersal syndrome). The evolutionary causes and consequences of such covariation depend on the degree of plasticity versus inheritance of the traits, which requires challenging experiments to implement in mobile organisms. Here, we combine a forced dispersal experiment, natural colonization and longitudinal data to establish if dispersal and aggression levels are integrated and to test their adaptive nature in pied flycatchers (Ficedula hypoleuca). We found that (forced) dispersers behaved more aggressively in their first breeding year after dispersal and decreased their aggression in following years. Strength of dispersal syndrome and direction of fecundity selection on aggression in newly colonized areas varied between years. We propose that the net benefits of aggression for dispersers increase under harsh conditions (e.g. low food abundance). This hypothesis now warrants further testing. Overall, this study provides unprecedented experimental evidence that dispersal syndromes can be remodelled via adaptive plasticity depending on the individuals' local breeding experience and/or year-specific ecological conditions. It highlights the importance of individual behavioural variation in population dynamics.

Sexual differences in phenotypical predictors of floating status: body condition influences male but not female reproductive status in a wild passerine

Floaters constitute the sexually mature but non-breeding part of populations. Despite being ubiquitous in most species, knowledge about floaters is scarce. Ignoring this significant number of individuals may strongly bias our understanding of population dynamics and sexual selection processes. We used the spotless starling (Sturnus unicolor) to examine whether phenotypical and non-phenotypical variables from early and adult life predict reproductive status, focusing on the earliest age at which most individuals start to breed, when the percentage of floaters is the highest. We compiled data from a long-term study involving eight female and seven male cohorts of individuals PIT-tagged at birth. We compared a suite of nestling (condition, hatching date and brood size) and adult variables (condition, size and ornamentation) between floaters and breeders. We found that adult and nestling body condition strongly and positively influenced the likelihood of breeding in males. Path analysis revealed that male reproductive status could only be predicted by considering nestling body condition—the influence of this variable superseded adult body condition. Female reproductive status was only negatively associated with hatching date. Ornamentation was not associated with reproductive status in any of the sexes, although path analyses revealed that body condition was positively associated with throat feather length. We conclude that predictors of reproductive status are sex-specific in the spotless starling, suggesting an important role of body condition in access to breeding resources in males. Our results also highlight the long-term influence of early life on life trajectories and their potential implications on floating status.

What is the best fitness measure in wild populations? A case study on the power of short-term fitness proxies to predict reproductive value.

Fitness is at the core of evolutionary theory, but it is difficult to measure accurately. One way to measure long-term fitness is by calculating the individual’s reproductive value, which represents the expected number of allele copies an individual passes on to distant future generations. However, this metric of fitness is scarcely used because the estimation of individual’s reproductive value requires long-term pedigree data, which is rarely available in wild populations where following individuals from birth to death is often impossible. Wild study systems therefore use short-term fitness metrics as proxies, such as the number of offspring produced. This study compared two frequently used short-term metrics for fitness obtained at different offspring life stages (eggs, hatchlings, fledglings and recruits), and compared their ability to predict reproductive values derived from the genetic pedigree of a wild passerine bird population. We used twenty years of precise field observations and a near-complete genetic pedigree to calculate reproductive success, individual growth rate and de-lifed fitness as lifetime fitness measures, and as annual de-lifed fitness. We compared the power of these metrics to predict reproductive values and lineage survival to the end of the study period. The three short-term fitness proxies predict the reproductive values and lineage survival only when measured at the recruit stage. There were no significant differences between the different fitness proxies at the same offspring stages in predicting the reproductive values and lineage survival. Annual fitness at one year old predicted reproductive values equally well as lifetime de-lifed fitness. However, none of the short-term fitness proxies were strongly associated with the reproductive values. The commonly used short-term fitness proxies best predict long-term fitness when measured at recruitment stage. Thus, because lifetime fitness measured at recruit stage and annual fitness in the first year of life were the best proxies of long-term fitness in short-lived birds, we encourage their future use.

Inbreeding is associated with shorter early-life telomere length in a wild passerine

Inbreeding can have negative effects on survival and reproduction, which may be of conservation concern in small and isolated populations. However, the physiological mechanisms underlying inbreeding depression are not well-known. The length of telomeres, the DNA sequences protecting chromosome ends, has been associated with health or fitness in several species. We investigated effects of inbreeding on early-life telomere length in two small island populations of wild house sparrows (Passer domesticus) known to be affected by inbreeding depression. Using genomic measures of inbreeding we found that inbred nestling house sparrows (n = 371) have significantly shorter telomeres. Using pedigree-based estimates of inbreeding we found a tendency for inbred nestling house sparrows to have shorter telomeres (n = 1195). This negative effect of inbreeding on telomere length may have been complemented by a heterosis effect resulting in longer telomeres in individuals that were less inbred than the population average. Furthermore, we found some evidence of stronger effects of inbreeding on telomere length in males than females. Thus, telomere length may reveal subtle costs of inbreeding in the wild and demonstrate a route by which inbreeding negatively impacts the physiological state of an organism already at early life-history stages.

Telomere length declines with age, but relates to immune function independent of age in a wild passerine.

Telomere length (TL) shortens with age but telomere dynamics can relate to fitness components independent of age. Immune function often relates to such fitness components and can also interact with telomeres. Studying the link between TL and immune function may therefore help us understand telomere–fitness associations. We assessed the relationships between erythrocyte TL and four immune indices (haptoglobin, natural antibodies (NAbs), complement activity (CA) and heterophil-lymphocyte (HL) ratio; n = 477–589), from known-aged individuals of a wild passerine (Malurus coronatus). As expected, we find that TL significantly declined with age. To verify whether associations between TL and immune function were independent of parallel age-related changes (e.g. immunosenescence), we statistically controlled for sampling age and used within-subject centring of TL to separate relationships within or between individuals. We found that TL positively predicted CA at the between-individual level (individuals with longer average TL had higher CA), but no other immune indices. By contrast, age predicted the levels of NAbs and HL ratio, allowing inference that respective associations between TL and age with immune indices are independent. Any links existing between TL and fitness are therefore unlikely to be strongly mediated by innate immune function, while TL and immune indices appear independent expressions of individual heterogeneity.

Circulation of zoonotic flaviviruses in wild passerine birds in Western Spain

We explore the presence of zoonotic flaviviruses (West Nile virus (WNV) and Usutu virus (USUV)) neutralizing antibodies in rarely studied passerine bird species. We report, for the first time in Europe, WNV-specific antibodies in red avadavat and cetti’s warbler, and USUV in yellow-crowned bishop. The evidence of WNV and USUV circulating in resident and migratory species has implications for both animal and public health. Future outbreaks in avian reservoir hosts may occur and passerines should be considered as priority target species in flavivirus surveillance programmes.

Diagnostic accuracy of seven radiographic views, alone and in combination, for diagnosis of pectoral girdle fractures in wild passerines after window collisions.

To determine the prevalence of pectoral girdle fractures in wild passerines found dead following presumed window collision and evaluate the diagnostic accuracy of various radiographic views for diagnosis of pectoral girdle fractures. Cadavers of 103 wild passerines that presumptively died as a result of window collisions. Seven radiographic projections (ventrodorsal, dorsoventral, lateral, and 4 oblique views) were obtained for each cadaver. A necropsy was then performed, and each bone of the pectoral girdle (coracoid, clavicle, and scapula) was evaluated for fractures. Radiographs were evaluated in a randomized order by a blinded observer, and results were compared with results of necropsy. Fifty-six of the 103 (54%) cadavers had ≥ 1 pectoral girdle fracture. Overall accuracy of using individual radiographic projections to diagnose pectoral girdle fractures ranged from 63.1% to 72.8%, sensitivity ranged from 21.3% to 51.1%, and specificity ranged from 85.7% to 100.0%. The sensitivity of using various combinations of radiographic projections to diagnose pectoral girdle fractures ranged from 51.1% to 66.0%; specificity ranged from 76.8% to 96.4%. Radiography alone appeared to have limited accuracy for diagnosing fractures of the bones of the pectoral girdle in wild passerines after collision with a window. Both individual radiographic projections and combinations of projections resulted in numerous false negative but few false positive results.

Experimental ghrelin administration affects migratory behaviour in a songbird

Twice a year, billions of birds take on drastic physiological and behavioural changes to migrate between breeding and wintering areas. On migration, most passerine birds regularly stop over along the way to rest and refuel. Endogenous energy stores are not only the indispensable fuel to complete long distance flights, but are also important peripheral signals that once integrated in the brain modulate crucial behavioural decisions, such as the decision to resume migration after a stopover. A network of hormones signals metabolic fuel availability to the brain in vertebrates, including the recently discovered gut-hormone ghrelin. Here, we show that ghrelin takes part in the control of migratory behaviour during spring migration in a wild migratory passerine. We manipulated blood concentrations of ghrelin of 53 yellow-rumped warblers (Setophaga coronata coronata) caught during stopover and automatically radio-tracked their migratory behaviour following release. We found that injections of acylated and unacylated ghrelin rapidly induced movements away from the release site, indicating that the ghrelin system acts centrally to mediate stopover departure decisions. The effects of the hormone manipulation declined within 8 h following release, and did not affect the overall rate of migration. These results provide experimental evidence for a pivotal role of ghrelin in the modulation of behavioural decisions during migration. In addition, this study offers insights into the regulatory functions of metabolic hormones in the dialogue between gut and brain in birds.

Individual variation in reaction norms but no directional selection in reproductive plasticity of a wild passerine population.

In the plant–insect–insectivorous bird food chain, directional changes in climate can result in mismatched phenology, potentially affecting selection pressures. Phenotypic plasticity in the timing of breeding, characterized by reaction norm slopes, can help maximize fitness when faced with earlier prey emergence. In temperate passerines, the timing of tree budburst influences food availability for chicks through caterpillar phenology and the resulting food abundance patterns. Thus, the timing of tree budburst might serve as a more direct proxy for the cue to time egg‐laying. The evolutionary potential of breeding plasticity relies on heritable variation, which is based upon individual variation, yet studies on individual variation in plasticity are few. Here, we tested for the laying date—budburst date and the clutch size—laying date reaction norms, and examined 1) the among‐individual variance in reaction norm intercepts and slopes; and 2) the selection differentials and gradients on these intercepts and slopes. Using long‐term data of oak (genus Quercus) budburst and blue tit (Cyanistes caeruleus) reproduction, we applied within‐subject centering to detect reaction norms, followed by bivariate random regression to quantify among‐individual variance in reaction norm properties and their covariance with fitness. Individuals significantly differed in intercepts and slopes of both laying date—budburst date and clutch size—laying date reaction norms, and directional selection was present for an earlier laying date and a larger clutch size (intercepts), but not on plasticity (slopes). We found that individuals have their own regimes for adjusting egg‐laying and clutch size. This study provides further support of individual variation of phenotypic plasticity in birds.

Artificial size selection experiment reveals telomere length dynamics and fitness consequences in a wild passerine.

Telomere dynamics could underlie life-history trade-offs among growth, size and longevity, but our ability to quantify such processes in natural, unmanipulated populations is limited. We investigated how 4years of artificial selection for either larger or smaller tarsus length, a proxy for body size, affected early-life telomere length (TL) and several components of fitness in two insular populations of wild house sparrows over a study period of 11years. The artificial selection was expected to shift the populations away from their optimal body size and increase the phenotypic variance in body size. Artificial selection for larger individuals caused TL to decrease, but there was little evidence that TL increased when selecting for smaller individuals. There was a negative correlation between nestling TL and tarsus length under both selection regimes. Males had longer telomeres than females and there was a negative effect of harsh weather on TL. We then investigated whether changes in TL might underpin fitness effects due to the deviation from the optimal body size. Mortality analyses indicated disruptive selection on TL because both short and long early-life telomeres tended to be associated with the lowest mortality rates. In addition, there was a tendency for a negative association between TL and annual reproductive success, but only in the population where body size was increased experimentally. Our results suggest that natural selection for optimal body size in the wild may be associated with changes in TL during growth, which is known to be linked to longevity in some bird species.

Short- and Long-Term Effects of Nutritional State on IGF-1 Levels in Nestlings of a Wild Passerine

Short- and Long-Term Effects of Nutritional State on IGF-1 Levels in Nestlings of a Wild Passerine

Short- and Long-Term Effects of Nutritional State on IGF-1 Levels in Nestlings of a Wild Passerine

Short- and Long-Term Effects of Nutritional State on IGF-1 Levels in Nestlings of a Wild Passerine

Heterothermy in a Small Passerine: Eastern Yellow Robins Use Nocturnal Torpor in Winter

Torpor is a controlled reduction of metabolism and body temperature, and its appropriate use allows small birds to adapt to and survive challenging conditions. However, despite its great energy conservation potential, torpor use by passerine birds is understudied although they are small and comprise over half of extant bird species. Here, we first determined whether a free-living, small ∼20 g Australian passerine, the eastern yellow robin (Eopsaltria australis), expresses torpor by measuring skin temperature (Ts) as a proxy for body temperature. Second, we tested if skin temperature fluctuated in relation to ambient temperature (Ta). We found that the Ts of eastern yellow robins fluctuated during winter by 9.1 ± 3.9°C on average (average minimum Ts 30.1 ± 2.3°C), providing the first evidence of torpor expression in this species. Daily minimum Ts decreased with Ta, reducing the estimated metabolic rate by as much as 32%. We hope that our results will encourage further studies to expand our knowledge on the use of torpor in wild passerines. The implications of such studies are important because species with highly flexible energy requirements may have an advantage over strict homeotherms during the current increasing frequency of extreme and unpredictable weather events, driven by changing climate.

Genetic architecture and heritability of early-life telomere length in a wild passerine.

Early-life telomere length (TL) is associated with fitness in a range of organisms. Little is known about the genetic basis of variation in TL in wild animal populations, but to understand the evolutionary and ecological significance of TL it is important to quantify the relative importance of genetic and environmental variation in TL. In this study, we measured TL in 2746house sparrow nestlings sampled across 20years and used an animal model to show that there is a small heritable component of early-life TL (h2 =0.04). Variation in TL among individuals was mainly driven by environmental (annual) variance, but also brood and parental effects. Parent-offspring regressions showed a large maternal inheritance component in TL ( =0.44), but no paternal inheritance. We did not find evidence for a negative genetic correlation underlying the observed negative phenotypic correlation between TL and structural body size. Thus, TL may evolve independently of body size and the negative phenotypic correlation is likely to be caused by nongenetic environmental effects. We further used genome-wide association analysis to identify genomic regions associated with TL variation. We identified several putative genes underlying TL variation; these have been inferred to be involved in oxidative stress, cellular growth, skeletal development, cell differentiation and tumorigenesis in other species. Together, our results show that TL has a low heritability and is a polygenic trait strongly affected by environmental conditions in a free-living bird.

A citizen science-based survey of avian mortality focusing on haemosporidian infections in wild passerine birds

BackgroundHaemosporidioses are common in birds and their manifestations range from subclinical infections to severe disease, depending on the involved parasite and bird species. Clinical haemosporidioses are often observed in non-adapted zoo or aviary birds, whereas in wild birds, particularly passerines, haemosporidian infections frequently seem to be asymptomatic. However, a recent study from Austria showed pathogenic haemosporidian infections in common blackbirds due to high parasite burdens of Plasmodium matutinum LINN1, a common parasite in this bird species, suggesting that virulent infections also occur in natural hosts. Based on these findings, the present study aimed to explore whether and to what extent other native bird species are possibly affected by pathogenic haemosporidian lineages, contributing to avian morbidity.MethodsCarcasses of passerine birds and woodpeckers were collected during a citizen science-based survey for avian mortality in Austria, from June to October 2020. Tissue samples were taken and examined for haemosporidian parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon by nested PCR and sequencing the mitochondrial cytb barcode region, histology, and chromogenic in situ hybridization applying genus-specific probes.ResultsFrom over 160 dead bird reportings, 83 carcasses of 25 avian species were submitted for investigation. Overall haemosporidian infection rate was 31%, with finches and tits prevailing species counts and infections. Sequence analyses revealed 17 different haplotypes (4 Plasmodium, 4 Haemoproteus, 9 Leucocytozoon), including 4 novel Leucocytozoon lineages. Most infected birds presented low parasite burdens in the peripheral blood and tissues, ruling out a significant contribution of haemosporidian infections to morbidity or death of the examined birds. However, two great tits showed signs of avian malaria, suggesting pathogenic effects of the detected species Plasmodium relictum SGS1 and Plasmodium elongatum GRW06. Further, exo-erythrocytic tissue stages of several haemosporidian lineages are reported.ConclusionsWhile suggesting generally little contribution of haemosporidian infections to mortality of the investigated bird species, the findings indicate a possible role of certain haemosporidian lineages in overall clinical manifestation, either as main causes or as concurrent disease agents. Further, the study presents new data on exo-erythrocytic stages of previously reported lineages and shows how citizen science can be used in the field of haemosporidian research.Graphic abstract

A Preliminary Assessment of the Potential Health and Genetic Impacts of Releasing Confiscated Passerines Into the Wild: A Reduced-Risk Approach.

The illegal capture and trade of wild birds have long been threats to biodiversity. The rehabilitation and release of confiscated animals may be a useful conservation tool in species management. However, differences between populations regarding health (e.g., different pathogens) and adaptation (e.g., local adaptation) must be taken into account, since both can negatively impact the recipient population. In this pilot study, we used two of the most illegally trafficked Brazilian wild passerine species, namely the red-crested cardinal (Paroaria coronata) and green-winged saltator (Saltator similis) as case studies and assessed some of the health threats that the release of confiscated passerines may pose to free-living birds. We also investigated the level of difference in mitochondrial genetic structure among populations living in different ecoregions. Blood, feces, and oropharyngeal swabs from confiscated (n = 115) and free-living (n = 120) passerines from the release sites were tested for the Newcastle disease virus, Salmonella spp., and Mycoplasma gallisepticum. These are considered major avian diseases by the Brazilian National Avian Health Program. We analyzed mtDNA to study the difference in genetic structure between populations using samples from 127 free-living passerines. We found no evidence of the Newcastle disease virus or Salmonella spp. in confiscated or free-living passerines from either species. However, the levels of infection with M. galissepticum detected in our study for red-crested cardinals and green-winged saltators calls for a high degree of caution in captive release programs. The difference in genetic structure between populations occurring in different regions was low, and was not significant between those from the Pampa/Subtropical Grasslands region. These results suggest that it may be possible to establish a cost-effective and sensitive protocol for releasing confiscated songbirds, provided that further genome-wide studies indicate that the functional genetic diversity among (at least some of the) populations is also low.

Phenotypic differences among wild passerine nestlings in relation to early-life rearing environment

Subtle changes in stress physiology during critical developmental stages have been linked to long-term fitness; however, the biological processes and phenotypic responses to early-life rearing environments, such as anthropogenic land use conditions, have not been fully evaluated in insectivorous birds. We manipulated Tree Swallow (Tachycineta bicolor (Vieillot, 1808)) brood sizes at sites with contrasting agricultural land use to assess phenotypic changes in body condition and genetic and physiological biomarkers of stress during the sensitive nestling growth phase. We predicted that nestling swallows raised on cropland-dominated sites, especially those in enlarged broods, would have lower body condition, shorter telomeres, and higher feather corticosterone than nestlings raised in smaller broods at grassland sites. Body condition was highest among nestlings raised in reduced broods but was unrelated to land use. Telomere lengths tended to be shorter in nestlings from enlarged broods and at cropland sites. Corticosterone was not related to any factor. Locally abundant insect populations associated with wetlands may have dampened the effects and (or) parent swallows assumed higher costs of reproduction rather than passing these costs to nestlings. Results suggest that food or other environmental stressors could reduce fledgling survival via telomere shortening; a hypothesis that requires further investigation due to its potential importance to population viability in multiple declining aerial insectivore species.