Vermilion Flycatcher Research Articles

Genome Assembly of Pyrocephalus nanus: A Step Toward the Genetic Conservation of the Endangered Little Vermilion Flycatcher of the Galapagos Islands.

Incredibly powerful whole genome studies of conservation genetics, evolution, and biogeography become possible for non-model organisms when reference genomes are available. Here, we report the sequence and assembly of the whole genome of the little vermilion flycatcher (Pyrocephalus nanus; family Tyrannidae), which is an endemic, endangered, and declining species of the Galapagos Islands. Using PacBio HiFi reads to assemble long contigs and Hi-C reads for scaffolding, we assembled a genome of 1.07 Gb comprising 267 contigs in 152 scaffolds, scaffold N50 74 M, contig N50 17.8 M, with 98.9% assigned to candidate chromosomal sequences and 99.72% of the BUSCO passeriformes 10,844 single-copy orthologs present. In addition, we used the novel HiFiMiTie pipeline to fully assemble and verify all portions of the mitochondrial genome from HiFi reads, obtaining a mitogenome of 17,151 bases, containing 13 protein-coding genes, 22 tRNAs, 2 rRNAs, two control regions, and a unique structure of control region duplication and repeats. These genomes will be a critical tool for much-needed studies of phylogenetics, population genetics, biogeography, and conservation genetics of Pyrocephalus and related genera. This genome and other studies that use it will be able to provide recommendations for conservation management, taxonomic improvement, and to understand the evolution and diversification of this genus within the Galapagos Islands.

Associations between bird song attributes and noise, light, date, and temperature: Vermilion flycatchers (Pyrocephalus rubinus) sing shorter and higher pitched songs in territories with more artificial light at night

Urban noise and artificial light at night (ALAN) are global pollutants affecting animal acoustic communication. A previous study that measured noise, but not ALAN, found that vermilion flycatchers produce longer songs in noisier territories. A subsequent study in another population, that measured noise and ALAN, found that males emit longer songs in brighter, but not noisier, territories. The negative result could be due a lack of sufficient noise variation in the latter study. We evaluated the contribution of noise and ALAN on song length, provided sufficient variation in noise and ALAN. We also measured song peak frequency. During the dawn chorus, we recorded songs of 41 vermilion flycatchers in two populations (UNAM and PERM), and measured noise, ALAN, and temperature. For the population with sufficient noise and ALAN variation (UNAM), we confirmed that song length was positively associated with noise; it was also negatively associated with ALAN, especially in those males recorded late in the breeding season. At UNAM, we found an overall positive association between song pitch and ALAN; additionally, males singing at relatively low ambient temperatures (12-15 °C) produced higher pitched songs as ALAN increased. Those singing closer to new moon and at relatively low ambient noise levels (43-54 dB[A]) sang higher pitched songs in brighter territories; these two results should be taken cautiously. Our results show that light, noise, date, and temperature are associated in unexpected ways with song length and pitch, potentially affecting song information content and sexual selection.

Habitat restoration to conserve the Little Vermilion Flycatcher on Santa Cruz Island, Galapagos.

The endemic Little Vermilion Flycatcher (LVF), Pyrocephalus nanus, has suffered a drastic decline on Santa Cruz Island, where it was common 30 years ago. Currently, less than 40 individuals remain in the last remnants of natural humid forest in the Galapagos National Park on this island. This small population has low reproductive success, which is contributing to its decline in Santa Cruz. Previous studies have identified Avian Vampire Fly, Philornis downsi, parasitism, changes in food sources, and habitat alteration as threats to this species. In Santa Cruz, invasive plants may strongly affect the reproductive success of the LVF because they limit accessibility to prey near the ground, the preferred foraging niche of these birds. Since 2019, we restored the vegetation in seven plots of one hectare each by removing invasive blackberry plants and other introduced plant species. In all nests that reached late incubation, we also reduced the number of Avian Vampire Fly larvae. In this study, we compared foraging and perch height, pair formation, incubation time and reproductive success between managed and unmanaged areas. As predicted, we found significantly lower foraging height and perch height in 2021 in managed areas compared to unmanaged areas. In 2020, daily failure rate (DFR) of nests in the egg stage did not differ between management types; however, in 2021, DFR in the egg stage was significantly lower in managed areas than in unmanaged areas. The DFR during the nestling stage was similar between managed and unmanaged areas in 2020, but in 2021, only nests in managed areas reached the nestling stage. Females brooded significantly more during the incubation phase in managed areas. Additionally, we found significantly higher reproductive success in managed areas compared to unmanaged areas in 2021, but not in 2020. Habitat restoration is a long-term process and these findings suggest that habitat management positively affects this small population in the long term.

New avian hosts for Taphropiestes plaumanni (Coleoptera: Cavognathidae) and the record of nestlings skin lesions and body deterioration associated with parasitism

We collected data during three consecutive breeding seasons (2015-2018) to assess the effects of Taphropiestes plaumanni (Coleoptera: Cavognathidae) on its bird hosts in a native forest of central eastern Argentina. We monitored bird nests for T. plaumanni in 207 nests of Masked Gnatcatcher (Polioptila dumicola, Polioptilidae), 302 nests of Vermilion Flycatcher (Pyrocephalus rubinus, Tyrannidae), 55 nests of Blue-and-yellow Tanager (Pipraeidea bonariensis, Thraupidae), 99 nests of Small-billed Elaenia (Elaenia parvirostris, Tyrannidae), 23 nests of Yellow-browed Tyrant (Satrapa icterophrys, Tyrannidae), and other passerine species nesting in the same forest patches. We found 13 nests in which nestlings showed evidences of parasitism of which four species are new hosts for this parasite (Vermilion Flycatcher, Masked Gnatcatcher, Red-crested Cardinal Paroaria coronata, Thraupidae, and Fork-tailed Flycatcher Tyrannus savana). Skin lesions caused by T. plaumanni larvae consisted in lacerations and crusts on the belly and chest areas. In one parasitized nest of Vermilion Flycatcher and one parasitized nest of Masked Gnatcatcher we observed the death of nestlings after being parasitized. This study adds new species to the list of hosts for this parasite, reports nestling skin lesions in nests with T. plaumanni parasitism, and reports for the first time the death of parasitized nestlings.

Vermilion flycatchers avoid singing during sudden peaks of anthropogenic noise

Vermilion flycatchers avoid singing during sudden peaks of anthropogenic noise

Dietary ecology of two migrant flycatchers in habitats with and without cattle during the breeding season in central Argentina

Food selection is a key aspect of a bird's life history strategy, so understanding how birds respond to variation in food abundance is relevant to evaluating their general ecology and survival, and also the potential consequences of the degradation of environments impacted by livestock. We studied the dietary ecology of Vermilion Flycatchers (VEFL) and Fork-tailed Flycatchers (FTFL), two insectivores and Neotropical austral migrants, during their breeding season. We worked in areas with and without cattle ranching in the Espinal biome of La Pampa, Argentina. We found different arthropod prey abundance for both flycatchers according to arthropod orders and/or study sites, suggesting that livestock may impact food abundance. Both consumed similar prey and positively selected for hymenopterans and coleopterans, and FTFL also positively selected for orthopterans. VEFL selected nest sites with a lower abundance of heteropterans and FTFL selected sites with a higher abundance of coleopterans. Additionally, VEFL nest survival was negatively related to the abundance of hemipterans and FTFL nest survival was positively related to the abundance of coleopterans. This study helps fill gaps on the general ecology of species that breed in rangelands, and highlights the importance of similar studies to formulate effective conservation planning for the Espinal biome.

More extinctions on the Galápagos Islands? An unsuccessful search for 4 landbirds on Floreana

Previous intensive surveys on Floreana, the smallest inhabited island of the Galápagos archipelago, in 2015 and 2016, produced reliable population estimates for all landbirds but failed to find 4 species that formerly occurred on the island: Gray Warbler Finch (Certhidea fusca), Vegetarian Finch (Platyspiza crassirostris), Little Vermilion Flycatcher (Pyrocephalus nanus), and Galápagos Rail (Laterallus spilonota). We revisited the island in February 2018 to extend our search to additional areas but again found none of the 4 lost species. As there is no longer any suitable habitat, we are certain that Galápagos Rail is now extinct on Floreana. It is possible that the remaining 3 species still survive in pockets of habitat that have not yet been surveyed. The very distinct subspecies of Gray Warbler-Finch (C. f. ridgwayi) especially merits further investigation.

BODY CONDITION OF BREEDING VERMILION FLYCATCHERS (PYROCEPHALUS RUBINUS) VARIES BETWEEN AREAS WITH AND WITHOUT CATTLE RANCHING IN CENTRAL ARGENTINA

The body condition of birds may be conditioned by intrinsic (e.g., sex, age, migratory and breeding status) and extrinsic factors, such as anthropic activities (e.g., livestock raising). We describe the biometry and body condition of Vermilion Flycatchers (VEFL) according to sex and age and evaluate which factors best predict their body condition during the breeding season in the Espinal of central Argentina. The study area included “Parque Luro” Provincial Reserve and two nearby private ranches with livestock. We captured and banded VEFL using mist nets between October to February, from 2015 to 2019. We calculated the scaled mass indexes, which relates body mass to biometric measures (culmen, tarsus, and tail length, and wing chord) to choose the best indicator of body condition. As explanatory variables, we used the breeding condition of females in one model, breeding condition of males in another model, and in a final model we used date, year and site, and included all individuals. We banded 93 VEFL that did not vary according to age-dependent body size or reproductive condition. Nevertheless, females weighed more, had higher fat levels and shorter wings than males. The body condition was only explained by breeding site, being smaller in one ranch than the other ranch and the reserve. We highlight the importance of reserves and the need for further research to understand the ecological constraints that South American birds face, to promote their conservation.

Two new feather mites of the genus Trouessartia Canestrini, 1899 (Acariformes: Trouessartiidae) from tyrant flycatchers (Passeriformes: Tyrannidae) in Argentina

Two new species of the feather mite genus Trouessartia (Analgoidea: Trouessartiidae) are described from tyrant flycatchers (Tyrannidae) in Argentina: Trouessartia salvadori sp. nov. from the White-crested Tyrannulet Serpophaga subcristata (Vieillot) and T. gonzalezacunai sp. nov. from the Vermilion Flycatcher Pyrocephalus rubinus (Boddaert). Trouessartia salvadori sp. nov. is close to T. longiducta Hernandes et Valim, 2015 and most clearly differs from the latter in having, in males, the genital apparatus with wedge-shaped hyaline extensions and the anterior genital papillae situated more distant from the midline than posterior ones, and in females, setae h1 not extending beyond the margin of the interlobar membrane, and the posterior part of the hysteronotal shield bearing well outlined ovate lacunae except in the narrow median area. Trouessartia gonzalezacunai sp. nov. is similar to T. savanae Hernandes, 2014, but is distinguished from that species in having, in males, the terminal lamellae shaped as a fishtail, the epiandrum shaped as a goblet, the apophyses of adanal apodemes represented by thick spine-like tubercles, and in females, setae h1 minute spiculiform about 10 long, and the external copulatory tube shaped as a small rounded tubercle near the margin of interlobar membrane.

The Impacts of Parasitic Flies (Philornis spp.) on Nestlings of Three Passerines in a Southern Temperate Forest of Argentina

Philornis flies exert strong negative selection on avian host life histories. However, their possible influence at the southern limits of parasite distribution remains poorly studied. We collected data on Philornis parasitism (prevalence, parasite load and latency) during three consecutive breeding seasons of the Masked Gnatcatcher Polioptila dumicola, Vermilion Flycatcher Pyrocephalus rubinus and Blue-and-yellow Tanager Pipraeidea bonariensis in a south temperate forest in Argentina. We hypothesised that Philornis parasitism would negatively influence both the growth and survival of infected nestlings. Regarding body size differences among nestlings of these three host species, we predicted that nestling survival in parasitised nests and parasite load per nestling would be greater the larger the species, and that the number of growth parameters that differ between parasitised and non-parasitised nestlings would be greater the smaller the species. We monitored 564 nests and found prevalence to be 16.7% for the Masked Gnatcatcher, 30.1% for the Vermilion Flycatcher, and 37.9% for the Blue-and-yellow Tanager. Parasitism increased during the season for all three species. As predicted, for the three species, nestling survival was lower in parasitised nests (∼30%) than in non-parasitised nests (∼90%) and for each species, one or more growth parameters were significantly lower for parasitised nestlings compared to non-parasitised nestlings. Our prediction relating to host body size was partially supported since differences in parasite load only emerged in nests that produced fledglings, as well as in the extent of growth parameters affected. This is the first study providing detailed data of Philornis fly parasitism and how this parasite affects the fitness of three bird hosts at the southern limit of the parasite's distribution.—Gonzalez, E., Jauregui, A. & Segura, L.N. (2022). The impacts of parasitic flies (Philornis spp.) on nestlings of three passerines in a southern temperate forest of Argentina. Ardeola, 69: 3-20.

Urbanization levels are associated with the start of the dawn chorus in vermilion flycatchers in Colombia

Increased urbanization leads to the modification of animal behavior, including the start of the dawn chorus in birds. The beginning of the dawn chorus has been studied in relation to the level of urban noise and nocturnal artificial light in oscine birds, with few studies in suboscines. We evaluated a possible relationship between the start of the dawn chorus and different urbanization levels in a suboscine, the vermilion flycatcher (Pyrocephalus rubinus), in seven locations in the city of Armenia (Colombia). We categorized the urbanization level in each location according to its percentage of built structures, into low and high levels. Observations were made during pre-dawn, starting at 00:00 hr. During each visit we recorded maximum noise levels, artificial light at night (ALAN) and time of first song. Males inhabiting the high urbanization locations started the dawn chorus on average 101 min before sunrise, while males in low urbanization levels did so on average 38 min before. Neither noise level nor ALAN explained this difference. We discuss that, for suboscines, another urban-related factor (ambient temperature) may be a key factor driving the onset of dawn chorus.

High levels of natal philopatry and no difference in reproductive success between philopatric and non-philopatric songbirds breeding in a native forests of east-central Argentina

ABSTRACT Philopatric birds have a number of advantages when breeding in familiar habitats, such as learning the locations of food, efficient movement throughout the breeding area, or effective escape from predators. However, few investigators have examined the possible effect of site familiarity on reproductive success, even less for Neotropical songbirds. We studied a breeding population of Masked Gnatcatchers (Polioptila dumicola) and Vermilion Flycatchers (Pyrocephalus rubinus), two south temperate songbirds, and examined the possible reproductive benefits of natal philopatry. In our population, 13.9% and 6.9% of breeding adults, respectively, for Masked Gnatcatchers and Vermilion Flycatchers, were philopatric. We found no difference in the breeding success between philopatric and non-philopatric individuals. Our results showed higher levels of philopatry for both species than previously reported for other songbirds. Because the remnants of native forests in our study area were located within a matrix of highly disturbed habitats, these intermediate-to-high values of natal philopatry could be linked to the structural characteristics of the forest that may force birds to use the few suitable forest patches available in the area.

Urbanization levels are associated with the start of the dawn chorus in vermilion flycatchers in Colombia

Urbanization levels are associated with the start of the dawn chorus in vermilion flycatchers in Colombia

Effect of an introduced parasite in natural and anthropogenic habitats on the breeding success of the endemic little vermilion flycatcher Pyrocephalus nanus in the Galápagos

In the Galápagos Islands many endemic bird species, including the emblematic Darwin's finches, show significant declines in population size. The endemic little vermilion flycatcher Pyrocephalus nanus, classified as vulnerable with high extinction risk, is strongly declining and broods regularly fail. We investigated multiple causes for breeding failure by comparing breeding success, infestation intensity by the hematophagous larvae of the introduced parasitic fly Philornis downsi, predation, parental food provisioning rate and prey attack rates as indicators of food availability at three study sites differing in anthropogenic habitat alterations: Alcedo on Isabela Island with its pristine habitat remote from human settlements, El Cura, also on Isabela Island but dominated by farmland, and Mina Roja on Santa Cruz Island, a site highly altered by introduced invasive plant species, mainly the blackberry. To test for the causal role of parasitism, we reduced the number of P. downsi larvae in half the nests at each site on Isabela Island, and used the other nests as control. When infestation intensity was experimentally reduced, both breeding success and food provisioning rates increased significantly in El Cura, but not in Alcedo, where breeding success and food provisioning rates were overall higher and infestation intensity lower than in El Cura. In the very small population of the little vermilion flycatcher in Mina Roja most nests were abandoned during the incubation phase before nests were infested by P. downsi. Mammalian predation played a minor role in brood loss at all three study sites. Our experimental study demonstrates that the recently introduced parasitic fly significantly affects breeding success of an endangered endemic bird species, and suggests that the effects are modulated by natural levels of P. downsi infestation and habitat‐related rates of food provisioning. Conservation measures should include P. downsi control combined with creating and maintaining open foraging areas.

Nest-site selection and breeding success of two neotropical austral migrant birds in a semiarid forest: A comparison of sites with and without livestock

Understanding the mechanisms underpinning nest-site selection offers novel insights about selective forces shaping the breeding ecology of birds, and provides vital information for conservation planning. We evaluated and compared nest-site selection and breeding success of Vermilion Flycatchers (VEFL) and Fork-tailed Flycatchers (FTFL) in areas with and without livestock in the Espinal biome of La Pampa Province, Argentina. VEFL selected nest sites with greater tree cover, whereas FTFL nested in taller trees with narrower trunks. We found a weak positive effect of nest height, diameter of nest-support branches and the absence of livestock on VEFL nest survival, and a weak positive effect of nest orientation on FTFL nest survival. However, although some habitat characteristics varied between the two areas, nest site characteristics of both species in areas with and without livestock did not differ significantly. The nest survival was 12.7% for VEFL and 28.7% for FTFL, and did not differ significantly between these two flycatchers. The breeding ecology of these birds has likely been molded by a broad suite of selective pressures, such as severe weather, brood parasites and predators that characterize habitats in central Argentina.

Acoustic differentiation in a sub-oscine calls: females call with more entropy than males

We quantified variation at the individual, pair and sex levels in acoustic attributes of Vermilion Flycatcher (Pyrocephalus rubinus)’s peent calls. We recorded calls of 15 pairs during the breeding season, and analyzed seven acoustic measures encompassing temporal, frequency and entropy measures. We run Principal Component Analysis to reduce the number of acoustic parameters; the first three principal components (PCs: PC1, PC2, and PC3) were related to call frequency, call entropy and call duration, respectively. These PCs were further used in Discriminant Function Analysis (DFA), and logistic regressions. Although all three PCs varied more among than within individuals, the DFA correctly classified only 57% of males and 63% of females, casting doubts on the possibility that the peent functions as an individual marker. At the pair level, only PC1 (call frequency) differed among pairs; however, the DFA correctly classified only 6.7%. of pairs. At the sex level, male peents had lower values of PC2 (call entropy) than female peents; the DFA correctly classified 66.7% and 73.3% of individuals as males and females, respectively (mean correct classification 70%). Binary logistic regression confirmed that only call entropy differed between sexes, and correctly classified 73.3% of females and 80% of males. Our data show sexual acoustic dimorphism in the peent, and open the possibility that variation in peent entropy may allow for sex discrimination in this species.

Survival and extinction of breeding landbirds on San Cristóbal, a highly degraded island in the Galápagos

SummaryWe documented the consequences of large-scale habitat loss on a community of Galápagos native bird species on San Cristóbal island, based on point counts conducted between 2010 and 2017. Surprisingly, despite considerable habitat change and a variety of other threats, the landbirds of San Cristóbal have fared much better than on the neighbouring islands Floreana or Santa Cruz. While two species went extinct very soon after human colonisation, the majority have adapted well to subsequent vegetation change and habitat loss. The endemic San Cristóbal Mockingbird Mimus melanotis is more widespread than previously thought and its population seems to be stable since the 1980s. We thus propose a change in IUCN classification from ‘Endangered’ to ‘Near threatened’. We present evidence gained by interviewing locals which suggests that a small population of the Least Vermilion Flycatcher Pyrocephalus dubius, classified as ‘Extinct’ by BirdLife International, may have persisted until very recently. Although extensive searches in 2018 and 2019 were unsuccessful, the possibility remains that a few birds may have survived in remote parts of the island. Further searches that involve the general public and other interested parties are therefore deemed necessary.

Territorial responses to song components in a suboscine, the vermilion flycatcher

Vermilion flycatchers songs are composed of two acoustically different parts: a first part (FP) containing a variable number of introductory elements, and a second part (SP) composed of four elements. Previous work suggests that the FP is important for territorial competition and that it conveys information on threat level. By exposing free-living males to playbacks of complete songs (CS’s), FP’s and SP’s, we evaluated the relative contribution of each song part in males’ territorial responses. Males called in response to all three treatments, suggesting each song component is important for territorial competition. Males’ call response did not differ toward CS’s and FP’s, and toward CS’s and SP’s (although a non-significant tendency was found for SP’s to elicit a weaker response than CS’s), but it was greater toward FP’s than toward SP’s. These results, coupled with previous work, further support the idea that the FP plays a special role during territorial competition and may give information on level of threat. We further discuss our result in terms of mechanistic and functional hypotheses.

No reliable evidence for immediate noise-induced song flexibility in a suboscine

Vermilion flycatchers, a suboscine, sing songs with more elements in territories with higher urban noise levels. We tested the hypothesis that this pattern is achieved through vocal flexibility, by which individuals add elements to their songs when noise increases; we also tested whether males modulate other song attributes and song output with noise. To this end, we did a playback experiment with free-living males where we recorded their songs during three noise treatments: first ambient noise (FAN), high urban noise (HUN), and second ambient noise (SAN) treatments. We counted the number of song elements and measured acoustic attributes both in the whole song and in the song terminal element (T). Males did not modify the number of song elements, nor song minimum frequency, with noise. The T minimum frequency slightly increased during SAN when compared to the FAN and HUN treatments, but it did not differ between the HUN and FAN treatments. Thus, we interpret these results as a lack of reliable evidence of immediate noise-induced song flexibility in frequency parameters. Song entropy decayed during the trials, but this seemed to be an effect of time and not a noise-induced change. Vermilion flycatchers appear to be less capable of modulating spectral song attributes to cope with noise than many oscines. We discuss other potential strategies that this species may use to deal with noise and a possible mechanism by which males end up singing longer songs in noisier territories (natural selection).

Phylogeography of the Vermilion Flycatcher species complex: Multiple speciation events, shifts in migratory behavior, and an apparent extinction of a Galápagos-endemic bird species

The Vermilion Flycatcher (Pyrocephalus rubinus) is a widespread species found in North and South America and the Galápagos. Its 12 recognized subspecies vary in degree of geographic isolation, phenotypic distinctness, and migratory status. Some authors suggest that Galápagos subspecies nanus and dubius constitute one or more separate species. Observational reports of distinct differences in song also suggest separate species status for the austral migrant subspecies rubinus. To evaluate geographical patterns of diversification and taxonomic limits within this species complex, we carried out a molecular phylogenetic analysis encompassing 10 subspecies and three outgroup taxa using mitochondrial (ND2, Cyt b) and nuclear loci (ODC introns 6 through 7, FGB intron 5). We used samples of preserved tissues from museum collections as well as toe pad samples from museum skins. Galápagos and continental clades were recovered as sister groups, with initial divergence at ∼1mya. Within the continental clade, North and South American populations were sister groups. Three geographically distinct clades were recovered within South America. We detected no genetic differences between two broadly intergrading North American subspecies, mexicanus and flammeus, suggesting they should not be recognized as separate taxa. Four western South American subspecies were also indistinguishable on the basis of loci that we sampled, but occur in a region with patchy habitat, and may represent recently isolated populations. The austral migrant subspecies, rubinus, comprised a monophyletic mitochondrial clade and had many unique nuclear DNA alleles. In combination with its distinct song, exclusive song recognition behavior, different phenology, and an isolated breeding range, our data suggests that this taxon represents a separate species from other continental populations. Mitochondrial and nuclear genetic data, morphology, and behavior suggest that Galápagos forms should be elevated to two full species corresponding to the two currently recognized subspecies, nanus and dubius. The population of dubius is presumed to be extinct, and thus would represent the first documented extinction of a Galápagos-endemic bird species. Two strongly supported mitochondrial clades divide Galápagos subspecies nanus in a geographic pattern that conflicts with previous hypotheses that were based on plumage color. Several populations of nanus have recently become extinct or are in serious decline. Urgent conservation measures should seek to preserve the deep mitochondrial DNA diversity within nanus, and further work should explore whether additional forms should be recognized within nanus. Ancestral states analysis based on our phylogeny revealed that the most recent common ancestor of extant Vermilion Flycatcher populations was migratory, and that migratory behavior was lost more often than gained within Pyrocephalus and close relatives, as has been shown to be the case within Tyrannidae as a whole.