European Passerines Research Articles

Empirically tuned theory reveals why symbiont abundance 'mite' vary across hosts.

Research Highlight: del Mar Labrador, M., Serrano, D., Doña, J., Aguilera, E., Arroyo, J. L., Atiénzar, F., Barba, E., Bermejo, A., Blanco, G., Borràs, A., Calleja, J. A., Cantó, J. L., Cortés, V., de la Puente, J., de Palacio, D., Fernández-González, S., Figuerola, J., Frías, Ó., Fuertes-Marcos, B. Garamszegi, L. Z., Gordo, Ó., Gurpegui, M., Kovács, I., Martínez, J. L., Meléndez, L., Mestre, A., Møller, A. P., Monrós, J. S., Moreno-Opo, R., Navarro, C., Pap, P. L., Pérez-Tris, J., Piculo, R., Ponce, C., Proctor, H., Rodríguez, R., Sallent, Á., Senar, J., Tella, J. L., Vágási, C. I., Vögeli, M., & Jovani, R. (2023). Host space, not energy or symbiont size, constrains feather mite abundance across passerine bird species. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.14032. Symbionts represent crucial links between species in ecosystems. Consequently, understanding their patterns of abundance is a major goal in the study of symbioses. However, multiple biotic and abiotic factors may regulate symbionts, and disentangling the mechanisms that drive variation in their abundance across host species is challenging. One promising strategy to approach this challenge is to incorporate biologically relevant data into theoretical models. In a recent study, Labrador etal. (2023) used this strategy to investigate the poorly understood symbiosis between feather mites and their avian hosts. They integrate a remarkable amount of empirical data with models based on the metabolic theory of ecology to determine what factors limit feather mite abundance across European passerines. Their quantitative analyses indicate that the number of feather barbs limits mite abundance across host species, suggesting that mite populations are spatially, but not energetically, constrained. These findings not only reveal mechanisms that may drive the variation in feather mite abundances across hosts, but also advance our understanding of the ecology of interspecific interactions more generally.

Consistent delay in recent timing of passerine autumn migration

Climate change affects important biological processes, bird migration phenology being a particular well-documented one. While spring migration have been found to advance by numerous studies, autumn migration is less studied and show more variable change in timing. Few studies of autumn migration are based on data from after 2000, leaving the last two decades to be relatively less studied. Here, we investigate recent change in autumn migration phenology of European passerines. The most recent available bird ringing data from Denmark is used to analyse phenological change of median and late migration of 14 passerine migrants between 2003–2021. We find an overall delay of autumn migration, mainly driven by short-distance migrants. All short-distance migrants, one out of five medium-distance and three out of five long-distance migrants delay autumn migration. None of the included species advance autumn migration significantly. As climate change has continuously resulted in milder conditions in north-western Europe, we expect this to cause further effects on migration phenology also in recent decades. Our results provide novel insight into recent migration phenology trends, and the observed delay in long-distance migrants may illustrate a changed response to climate change.

Effects of positive frequency-dependent learning, learning mistakes, and immigration on complex cultures–Validation on the song of collared flycatcher (Ficedula albicollis) by individual-based modeling

Cultural diversity and stability of a population affect the adaptiveness and survival of individuals. Besides field studies, cultural diversity and stability have been investigated with the help of different modeling approaches in relatively simple cultures. These theoretical studies helped identify mechanisms that generate cultural diversity through increasing the proportion of new elements in the population, for example by immigration or erroneous learning. Copy-the-majority learning strategies, forms of positive frequency-dependent learning, have a rather opposite effect: while they help in maintaining cultural stability by favoring the spread of common elements, they also decrease cultural diversity. We investigated whether these basic, conflicting mechanisms are sufficient together to create a complex, polymorphic cultural system and to maintain its diversity and stability. For that we developed an individual-based model simulating song learning in birds in which the extent of immigration, the frequency of learning mistakes and the strength of positive frequency-dependent learning were included as modifiable parameters. From the model, we obtained information on the composition and temporal changes in the individual and population repertoires. A comparison with long-term field data on a European passerine bird species with moderate song complexity, the collared flycatcher (Ficedula albicollis), was also performed. Our results confirmed that certain combinations of the three investigated mechanisms were indeed able to create patterns that showed certain aspects of polymorphic cultures. Yet, several discrepancies occurred when comparing the simulation results with the field data that emphasize the implementation of other mechanisms, especially those that have a stabilizing effect. Long-term metastable states, found in the population-level cultural diversity, raise awareness to animal cultures’ possible sensitivity to external factors.

Male song of the Aquatic Warbler, a promiscuous bird without paternal care, is more complex than previously thought

The Aquatic Warbler Acrocephalus paludicola is one of the rarest European passerines and is characterised by promiscuity, lack of pair-bonds and female-only parental care. This makes the species an important model for studying the function of avian courtship song. The song of the Aquatic Warbler consists of whistle and rattle phrases produced as discontinuous A-, B- and C-songs, which are built by a single rattle, a rattle and a whistle, and more than two phrases of both kinds, respectively. The A- and B-songs are thought to be aggressive signals in male-male interactions, while C-songs are thought to be important for female choice. Here, we analysed recordings of 40 individually marked males, and determined the phrase repertoire. The enumerated repertoire (males recorded for ≥ 10 min) ranged from 16 to 158 (mean 99), however, it did not capture the complete phrase repertoires. We then used models from species diversity ecology to estimate the actual phrase repertoire size, which ranged between 18 and 300 phrases (mean 155). The estimated repertoire was predicted by the number of C-songs. The rattle repertoire was larger than the whistle repertoire, and both positively correlated with the number of C-songs. Our study indicates that male Aquatic Warblers have highly complex phrase repertoires that vary widely in size. Their courtship song is flexible and efficient, enabling relative song complexity to be demonstrated in a short sample, thus facilitating both female attraction through the quick presentation of large phrase repertoires and rival deterrence through the production of many short and simple A- and B-songs.

Sexual selection, feather wear, and time constraints on the pre-basic molt explain the acquisition of the pre-alternate molt in European passerines.

Avian feathers need to be replaced periodically to fulfill their functions, with natural, social, and sexual selection presumably driving the evolution of molting strategies. In temperate birds, a common pattern is to molt feathers immediately after the breeding season, the pre‐basic molt. However, some species undergo another molt in winter‐spring, the pre‐alternate molt. Using a sample of 188 European passerine species, Bayesian phylogenetic mixed models, and correlated evolution analyses, we tested whether the occurrence of the pre‐alternate molt was positively associated with proxies for sexual selection (sexual selection hypothesis) and nonsexual social selection (social selection hypothesis), and with factors related to feather wear (feather wear hypothesis) and time constraints on the pre‐basic molt (time constraints hypothesis). We found that the pre‐alternate molt was more frequent in migratory and less gregarious species inhabiting open/xeric habitats and feeding on the wing, and marginally more frequent in species with strong sexual selection and those showing a winter territorial behavior. Moreover, an increase in migratory behavior and sexual selection intensity preceded the acquisition of the pre‐alternate molt. These results provide support for the feather wear hypothesis, partial support for the sexual selection and time constraints hypotheses, and no support for the social selection hypothesis.

Book Review

Book Review

The explosive radiation, intense host-shifts and long-term failure to speciate in the evolutionary history of the feather mite genusAnalges(Acariformes: Analgidae) from European passerines

AbstractMites of the genus Analges (Acariformes: Analgidae) inhabit the down feathers of passeriform birds. The evolutionary history of Analges and the co-phylogentic relationships between these mites and their hosts are unknown. Our phylogenetic analysis supported the monophyly of the genus, but it did not support previous taxonomic hypotheses subdividing the genus into the subgenera Analges and Analgopsis or arranging some species into the A. chelopus and A. passerinus species groups. Molecular data reveal seven new species inhabiting Eurasian passerines and support the existence of several multi-host species. According to molecular dating, the origin of the Analges (c. 41 Mya) coincided with the Eocene diversification of Passerida into Sylvioidea and Muscicapoidea–Passeroidea. The initial diversification of Analges took place on the Muscicapoidea clade, while remaining passerine superfamilies appear to have been colonized because of host-switching. Co-speciation appears to be relatively common among Analges species and their hosts, but the most striking pattern in the co-phylogenetic scenario involves numerous complete host-switches, spreads and several failures to speciate. The mechanism of long-term gene-flow among different populations of multi-host Analges species is enigmatic and difficult to resolve. Probably, in some cases mites could be transferred between birds via feathers used as nest material.

A revision of bird skin preparation aimed at improving the scientific value of ornithological collections

The methods used to preserve bird skins in museums have a potentially crucial impact on the feasibility and use of these specimens as a source of biological knowledge, although this subject is rarely broached. Study skins of birds are usually prepared with folded wings and straight legs to facilitate storage in the collection; yet, this method can hamper the measurement and examination of certain important features such as wing-feather moult. To make consultation easier for ornithologists, alternative preparation methods such as the splitting of wings and tarsi from the rest of the animal have been proposed by curators. Our aim was to study whether or not preparing bird specimens with spread limbs makes consultation simpler. First, we used two different methods to prepare two specimens each of two common European passerine species: (1) ‘traditional’ (folded wings and straight tarsi) and (2) ‘spread’ (limbs spread on one side of the body). Then, we asked 22 experienced ornithologists to identify moult limits and take three biometric measurements (wing chord, length of the third primary feather and tarsus length) from all four specimens. Subsequently, we asked which preparation method they preferred for obtaining data. The ‘spread’ preparation was preferred for moult, third primary feather length and tarsus length, whilst the ‘traditional’ preparation was preferred for wing chord. Data obtained from the folded and spread preparations were very highly repeatable within each method but only moderately to highly repeatable between methods. One of the handicaps with the ‘spread’ preparation is the increase in storage space required, a factor that should be taken into account before it is employed. Nevertheless, this specimen preparation technique can greatly facilitate consultation and therefore improve the scientific value of ornithological collections.

Discriminating between similar alarm calls of contrasting function.

In a pioneering study of signal design, Marler (Marler 1955 Nature176, 6-8. (doi:10.1038/176006a0); Marler 1957 Behaviour11, 13-37. (doi:10.1163/156853956X00066)) argued that the contrasting acoustic design of hawk (seet) and mobbing alarm calls of European passerines reflected their contrasting function. Hawk alarms were high-frequency tones, warning conspecifics to flee but making localization difficult for predators, while mobbing calls were broadband and harsh, allowing easy localization and approach. Contrasting signal features are also consistent with signal detection theory. Discriminating these calls quickly is critical for survival, because hawk alarms require immediate escape. These signals should therefore be selected to be easy to discriminate, reducing the trade-off between immediate fleeing to hawk alarms and unnecessary fleeing to mobbing alarms. Despite these expectations, hawk and mobbing alarm calls of superb fairy-wrens, Malurus cyaneus, are surprisingly similar, raising the question of discriminability without contextual cues. We synthesized these calls on computer, made intermediates and used playbacks to test whether calls can be discriminated acoustically, and if so by what features. We found that birds used multiple acoustic features when discriminating calls, allowing fast discrimination despite overlap in individual parameters. We speculate that the similarity of fairy-wren alarm calls could enhance detectability of both signals, while multiple subtle acoustic differences reduce a trade-off with discriminability. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

Post-Juvenile and Post-Breeding Moult of the Black Wheatear Oenanthe leucura in South-Eastern Spain: Slowed Down Due to Climatic Aridity?

Despite increasing interest in moult in birds, there are still clear gaps in our knowledge of this topic. For example, many aspects of the moult of several European passerines remain unknown. Here, I describe the extent of the postjuvenile and the post-breeding moult of Black Wheatears Oenanthe leucura in south-eastern Spain and analyse the possible influence of ecological factors on moult in this species. The post-juvenile moult of Black Wheatears involved a variable number of greater coverts (six in most cases), but tertials, alula feathers and the carpal covert were also moulted frequently. Primaries were never moulted, while secondaries and tail feathers were moulted in 1.5% of 65 birds. The number of feathers moulted in the post-juvenile moult was not related to sex or individuals' body size. The post-breeding moult occurred between late June and mid-November and followed the typical sequence of European passerines. It had a mean duration of 145 days, with no differences between sexes or years. The body condition of wheatears did not decrease as the moult advanced. The duration of the post-breeding moult of Black Wheatears was almost double the mean duration described for European passerines and is among the longest period ever described for passerines. The resident status and medium size of the species may partly explain the long duration of the post-breeding moult, but the low seasonality and high aridity of the study area seem to be the main drivers of the pattern found.

Dietary carotenoid supplementation facilitates egg laying in a wild passerine.

During egg laying, females face a trade‐off between self‐maintenance and investment into current reproduction, since providing eggs with resources is energetically demanding, in particular if females lay one egg per day. However, the costs of egg laying not only relate to energetic requirements, but also depend on the availability of specific resources that are vital for egg production and embryonic development. One of these compounds are carotenoids, pigments with immuno‐stimulatory properties, which are crucial during embryonic development. In this study, we explore how carotenoid availability alleviates this trade‐off and facilitates egg laying in a small bird species, the blue tit (Cyanistes caeruleus). Blue tits have among the largest clutch size of all European passerines and they usually lay one egg per day, although laying interruptions are frequent. We performed a lutein supplementation experiment and measured potential consequences for egg laying capacity and egg quality. We found that lutein‐supplemented females had less laying interruptions and thus completed their clutch faster than control females. No effects of treatment were found on the onset of egg laying or clutch size. Experimentally enhanced carotenoid availability did not elevate yolk carotenoid levels or egg mass, but negatively affected eggshell thickness. Our results provide hence evidence on the limiting role of carotenoids during egg laying. However, the benefits of laying faster following lutein supplementation were counterbalanced by a lower accumulation of calcium in the eggshell. Thus, even though single components may constrain egg laying, it is the combined availability of a range of different resources which ultimately determines egg quality and thus embryonic development.

Lasting the distance: The survival of alien birds shipped to New Zealand in the 19th century.

Invasive alien species are a major threat to biodiversity and human activities, providing a strong incentive to understand the processes by which alien invasion occurs. While it is important to understand the determinants of success at each of several invasion stages—transport, introduction, establishment, and spread—few studies have explored the first of these stages. Here, we quantify and analyze variation in the success of individual animals in surviving the transport stage, based on shipping records of European passerines destined for New Zealand. We mined the original documents of Acclimatisation Societies, established in New Zealand for the purpose of introducing supposedly beneficial alien species, in combination with recently digitized newspaper archives, to produce a unique dataset of 122 ships that carried passerines from Europe to New Zealand between 1850 and 1885. For 37 of these shipments, data on the survival of individual species were available. Using generalized linear mixed models, we explored how survival was related to characteristics of the shipments and the species. We show that species differed greatly in their survival, but none of the tested traits accounted for these differences. Yet, survival increased over time, which mirrors the switch from early haphazard shipments to larger organized shipments. Our results imply that it was the quality of care received by the birds that most affected success at this stage of the invasion process.

Ressenya [Moult and Ageing of European Passerines. London: Bloomsbury Publishing, 304 pp. Second Edition

Ressenya [Moult and Ageing of European Passerines. London: Bloomsbury Publishing, 304 pp. Second Edition

Enabling large-scale feather mite studies: an Illumina DNA metabarcoding pipeline.

Feather mites are among the most common and diverse ectosymbionts of birds, yet basic questions such as the nature of their relationship remain largely unanswered. One reason for feather mites being understudied is that their morphological identification is often virtually impossible when using female or young individuals. Even for adult male specimens this task is tedious and requires advanced taxonomic expertise, thus hampering large-scale studies. In addition, molecular-based methods are challenging because the low DNA amounts usually obtained from these tiny mites do not reach the levels required for high-throughput sequencing. This work aims to overcome these issues by using a DNA metabarcoding approach to accurately identify and quantify the feather mite species present in a sample. DNA metabarcoding is a widely used molecular technique that takes advantage of high-throughput sequencing methodologies to assign the taxonomic identity to all the organisms present in a complex sample (i.e., a sample made up of multiple specimens that are hard or impossible to individualise). We present a high-throughput method for feather mite identification using a fragment of the COI gene as marker and Illumina Miseq technology. We tested this method by performing two experiments plus a field test over a total of 11,861 individual mites (5360 of which were also morphologically identified). In the first experiment, we tested the probability of detecting a single feather mite in a heterogeneous pool of non-conspecific individuals. In the second experiment, we made 2 × 2 combinations of species and studied the relationship between the proportion of individuals of a given species in a sample and the proportion of sequences retrieved to test whether DNA metabarcoding can reliably quantify the relative abundance of mites in a sample. Here we also tested the efficacy of degenerate primers (i.e., a mixture of similar primers that differ in one or several bases that are designed to increase the chance of annealing) and investigated the relationship between the number of mismatches and PCR success. Finally, we applied our DNA metabarcoding pipeline to a total of 6501 unidentified and unsorted feather mite individuals sampled from 380 European passerine birds belonging to 10 bird species (field test). Our results show that this proposed pipeline is suitable for correct identification and quantitative estimation of the relative abundance of feather mite species in complex samples, especially when dealing with a moderate number (> 30) of individuals per sample.

MHC-mediated sexual selection on birdsong: Generic polymorphism, particular alleles and acoustic signals.

Several hypotheses predict that the major histocompatibility complex (MHC) drives mating preference in females. Olfactory, colour or morphological traits are often found as reliable signals of the MHC profile, but the role of avian song mediating MHC-based female choice remains largely unexplored. We investigated the relationship between several MHC and acoustic features in the collared flycatcher (Ficedula albicollis), a European passerine with complex songs. We screened a fragment of the class IIB second exon of the MHC molecule, of which individuals harbour 4-15 alleles, while considerable sequence diversity is maintained at the population level. To make statistical inferences from a large number of comparisons, we adopted both null-hypothesis testing and effect size framework in combination with randomization procedures. After controlling for potential confounding factors, neither MHC allelic diversity nor the presence of particular alleles was associated remarkably with the investigated qualitative and quantitative song traits. Furthermore, genetic similarity among males based on MHC sequences was not reflected by the similarity in their song based on syllable content. Overall, these results suggest that the relationship between features of song and the allelic composition and diversity of MHC is not strong in the studied species. However, a biologically motivated analysis revealed that individuals that harbour an MHC allele that impairs survival perform songs with broader frequency range. This finding suggests that certain aspects of the song may bear reliable information concerning the MHC profile of the individuals, which can be used by females to optimize mate choice.

David Pearson (1941–2017)

David Pearson (1941–2017)

Overwintering habitat links to summer reproductive success: intercontinental carry-over effects in a declining migratory bird revealed using stable isotope analysis

ABSTRACTCapsule: Breeding success in female Pied Flycatchers Ficedula hypoleuca is related to isotopic signature of feathers grown in Africa, suggesting wintering habitat links to breeding performance 5000 km away.Aims: Better understanding of inter-seasonal carry-over effects is a research priority, especially for declining migrants. We use stable isotope analysis to relate Pied Flycatcher winter habitat to summer reproductive success.Methods: Flycatchers were captured in three UK woodlands in 2013–15. An Africa-grown tertial was trimmed and analysed using Isotope Ratio Mass Spectrometry to quantify Nitrogen-15 (δ15N) and Carbon-13 (δ13C). In total, 135 samples were taken from 80 individuals.Results: Wintering δ15N and δ13C differed significantly between years. δ13C correlated with lay date, such that birds with lower carbon levels (indicative of more mesic habitat) bred earlier. There was a significant correlation between wintering δ13C and productivity after allowing for year, site and lay date; birds with low δ13C were more successful. This suggests δ13C links productivity directly as well as indirectly through phenological effects. δ15N did not relate to phenology or productivity.Conclusion: This is the first evidence of carry-over effects between geographical regions for a European passerine. Conservation measures should focus on all aspects of seasonal cycles, not just breeding grounds.

Cophylogenetic analyses reveal extensive host-shift speciation in a highly specialized and host-specific symbiont system

Host-shift speciation and cospeciation are the two major processes driving symbiont macroevolutionary diversification. Cospeciation is expected to be frequent in vertically transmitted and host-specific symbionts, and leads to congruent host-symbiont phylogenies. However, the cophylogenetic dynamics of many groups of highly specialized host-specific symbionts is largely unstudied. Thus, the relevance of cospeciation vs. host-shift speciation remains largely unknown. Here, we investigated this question by performing the largest cophylogenetic study of feather mites to date, using both distance and event-based cophylogenetic methods. For these analyses, we inferred phylogenies based on all protein coding genes of the mitochondrial genome of Proctophyllodes and Trouessartia feather mite species living on European passerine birds. Results show high incongruence among bird and feather mite phylogenies, because of extensive host-switching. We conclude that host-shift speciation, rather than cospeciation, may be the main driver of symbiont diversification even for highly specialized symbionts with low host-switching potential.

Mobbing calls: a signal transcending species boundaries

When they detect a predator, some prey exhibit mobbing behaviour and produce mobbing calls that quickly draw a mixed conspecific and heterospecific group against the predator. While the efficiency of this strategy is often linked to interspecific communication, it raises the question of how animals recognize these signals as mobbing calls. It is usually suggested that associative learning about a predator when heterospecific mobbing calls are heard plays a crucial role in communication among species. Alternatively, phylogenetic conservation or evolutionary convergence could also explain this communication process. To determine whether prior experience is required to express a mobbing response, we conducted playback experiments with four European passerine species: great tit, Parus major, blue tit, Cyanistes caeruleus, coal tit, Periparus ater, and common chaffinch, Fringilla coelebs. The aim of the study was to examine whether they would respond to the mobbing signals of several North American passerines. As expected, because natural selection might shape a strong response to conspecific mobbing calls, our focal species reacted more strongly towards their own mobbing calls than towards those of American species. Nevertheless, for the three European species of tit, prior experience of heterospecific mobbing calls was not required to elicit a response. Additionally, for great tit and chaffinch, we found that acoustic similarity could explain behavioural responses to allopatric species. In contrast, such similarity was probably not the main mechanism underlying the response for the other two European species. Heterospecific response to mobbing calls probably involved many different mechanisms. Further studies focusing on each of these should allow us to understand their relative contribution to heterospecific communication.

How weather instead of urbanity measures affects song trait variability in three European passerine bird species.

Previous studies detected an influence of urban characteristics on song traits in passerine birds, that is, song adjustments to ambient noise in urban areas. Several studies already described the effect of weather conditions on the behavior of birds, but not the effect on song traits. We investigate, if song trait variability changes along a continuous urbanity gradient in Frankfurt am Main, Germany. We examined, for the first time on a larger scale, the influence of weather on song parameters. We made song recordings of three common passerine species: the blue and great tit (Cyanistes caeruleus (Linnaeus, 1758) and Parus major Linnaeus, 1758) and the European blackbird (Turdus merula Linnaeus, 1758). We measured different song traits and performed statistical analyses and modeling on a variety of variables—among them urbanity and weather parameters. Remarkably, we found only few cases of a significant influence of urbanity parameters on song traits. The influence of weather parameters (air pressure, atmospheric humidity, air and soil temperatures) on song traits was highly significant. Birds in Frankfurt face high noise pollution and might show different adaptations to high noise levels. The song trait variability of the investigated species is affected more by weather conditions than by urban characteristics in Frankfurt. However, the three species react differently to specific weather parameters. Smaller species seem to be more affected by weather than larger species.