Suboscine Species Research Articles

The dynamics behind diversity in suboscine songs.

Vocal behavior plays a crucial evolutionary role. In the case of birds, song is critically important in courtship, male-male competition and other key behaviors linked to reproduction. However, under natural conditions, a variety of avian species live in close proximity and share an 'acoustic landscape'. Therefore, they need to be able to differentiate their calls or songs from those of other species and also from those of other individuals of the same species. To do this efficiently, birds display a remarkable diversity of sounds. For example, in the case of vocal learners, such as oscine passerines (i.e. songbirds), complex sequences and subtle acoustic effects are produced through the generation of complex neuromuscular instructions driving the vocal organ, which is remarkably conserved across approximately 4000 oscine species. By contrast, the majority of the sister clade of oscines, the suboscine passerines, are thought not to be vocal learners. Despite this, different suboscine species can generate a rich variety of songs and quite subtle acoustic effects. In the last few years, different suboscine species have been shown to possess morphological adaptations that allow them to produce a diversity of acoustic characteristics. Here, we briefly review the mechanisms of sound production in birds, before considering three suboscine species in more detail. The examples discussed in this Review, integrating biological experiments and biomechanical modeling using non-linear dynamical systems, illustrate how a morphological adaptation can produce complex acoustic properties without the need for complex neuromuscular control.

The delayed effect of climatic conditions on pre‐fledging nestling haematocrit in a suboscine species in Patagonia

Haematocrit, the proportion of blood comprising erythrocytes, is often used as a proxy of individual condition. Nestling haematocrit is influenced by several factors but ambient temperature is generally agreed as a key driver. It is unclear which day(s) in embryonic or nestling development are most influential in determining pre‐fledgling haematocrit. This is important, because if we are able to identify what day(s) nestlings are physiologically most vulnerable to climatic conditions, this may inform future conservation management and help mitigate the effects. We investigated the effect of ambient temperature, precipitation, body size, brood size, age, food abundance and habitat on nestling haematocrit in Aphrastura spinicauda (thorn‐tailed rayaditos). We collected this data from two climatically different locations in Chile: northern Patagonia (Pucón) and Sub‐Antarctic Patagonia (Navarino Island), located ~ 1800 km further south. We aimed to identify the key drivers of nestling haematocrit and find when nestlings are physiologically most vulnerable to climatic conditions. We confirm that ambient temperature is the key driver of nestling haematocrit, with increasing ambient temperatures nestling haematocrit decreased. However, precipitation also affected haematocrit in the late incubation stage. At low and high precipitation, nestling haematocrit was low and is optimum in light rainfall. Our results show a delayed effect of ambient temperature and precipitation in late incubation and on the day of hatching which can determine pre‐fledgling haematocrit, which may cause lower post‐fledgling fitness. We found that climatic conditions on the day haematocrit was collected was not important in determining haematocrit. We found that haematocrit was higher in the sub‐Antarctic area and that higher temperatures and precipitation on the day of hatching will result in lower nestling haematocrit and poorer pre‐fledgling condition. As atmospheric temperatures rise, nestling fitness is at risk. This is a threat to many bird species, especially those in locations vulnerable to climate breakdown.

Development syndromes in New World temperate and tropical songbirds.

We studied avian development in 49 to 153 species of temperate and tropical New World passerine birds to determine how growth rates, and incubation and nestling periods, varied in relation to other life-history traits. We collected growth data and generated unbiased mass and tarsus growth rate estimates (mass n = 92 species, tarsus n = 49 species), and measured incubation period (n = 151) and nestling period (n = 153), which we analyzed with respect to region, egg mass, adult mass, clutch size, parental care type, nest type, daily nest predation rate (DMR), and nest height. We investigated covariation of life-history and natural-history attributes with the four development traits after controlling for phylogeny. Species in our lowland tropical sample grew 20% (incubation period), 25% (mass growth rate), and 26% (tarsus growth rate) more slowly than in our temperate sample. Nestling period did not vary with respect to latitude, which suggests that tropical songbirds fledge in a less well-developed state than temperate species. Suboscine species typically exhibited slower embryonic and post-embryonic growth than oscine passerines regardless of their breeding region. This pattern of slow development in tropical species could reflect phylogenetic effects based on unknown physiological attributes. Time-dependent nest mortality was unrelated to nestling mass growth rate, tarsus growth rate, and incubation period, but was significantly associated with nestling period. This suggests that nest predation, the predominant cause of nest loss in songbirds, does not exert strong selection on physiologically constrained traits, such as embryonic and post-embryonic growth, among our samples of temperate and lowland tropical songbird species. Nestling period, which is evolutionarily more labile than growth rate, was significantly shorter in birds exposed to higher rates of nest loss and nesting at lower heights, among other traits. Differences in life-history variation across latitudes provide insight into how unique ecological characteristics of each region influence physiological processes of passerines, and thus, how they can shape the evolution of life histories. While development traits clearly vary with respect to latitude, trait distributions overlap broadly. Life-history and natural history associations differ for each development trait, which suggests that unique selective pressures or constraints influence the evolution of each trait.

Symmetrical discrimination despite weak song differentiation in 2 suboscine bird sister species

Abstract Song mediates territorial competition and mate choice in birds and population divergence in this signal can have important evolutionary consequences. For example, divergent songs can act in specific recognition and limit gene flow and, hence, have a fundamental role on the origin and/or integrity of evolutionary lineages. Especially interesting systems to test the role of song in specific recognition are species pairs that present small structural differences in this signal. Here, we perform song play-back experiments on males of a long-diverged sister pair of Neotropical Suboscine species, the squamate antbird (Myrmoderus squamosus) and the white-bibbed antbird (Myrmoderus loricatus), which occur in parapatry in the Atlantic Forest and that overlap extensively in song variation. Previous evidence indicates that genetic introgression between these species is either absent or negligible, suggesting that vocal discrimination or other mechanisms function as effective barriers to gene flow. Our results show that responses to heterospecific songs were symmetrical and intermediary compared with responses to conspecific songs in both species. A stronger response to conspecific territorial songs suggests that conspecific individuals pose greater competitive threat than heterospecifics. An important implication of our study is that even small song differences can play an important role in specific recognition.

Vocal divergence between two disjunct populations of Giant Antshrike (Batara cinerea) is related to environmental conditions

AbstractVariation in the avian vocal signals emitted may have a significant impact on species evolution. Vocal divergence in suboscine species like Giant Antshrike (Batara cinerea) may be associated with selective adaptation, since learning has little influence on vocal development and variation in acoustic structure cannot be attributed to learning deviation. Consequently, tracheophone suboscine species are ideal subjects to explore vocal variation, since cultural evolution does not seem to influence vocal variation in this group. Environmental conditions may determine the selection of vocal features because acoustic transmission could be attenuated under certain conditions of temperature, humidity and vegetation cover. Here, we examined vocalizations of Giant Antshrike and assessed possible acoustic variations between two disjunct groups (Andean and Atlantic), correlating the differences to the environmental structure. Univariate and multivariate analysis show temporal and spectral differences between both groups. Andean individuals produce vocalizations with longer duration, faster trill rates, shorter syllable duration and higher frequencies. Environmental features are different between the two populations, and they are correlated to the acoustic structure of vocalizations. Temporal variations arise directly from climatic influence, while spectral divergence could be a secondary effect of morphological adaptation to habitat structure.

Birdsong characteristics are related to fragment size in a neotropical forest

The oscine passerines, an avian suborder that comprises almost half of all bird species worldwide, learn their song primarily through cultural transmission. As the world's forests become increasingly fragmented and the population sizes of many forest-dwelling species decline, there may be increasingly restricted opportunities for the transmission of cultural information. However, the effects of forest fragmentation on birdsong have not been well documented. In this paper, we examine the relationship between forest fragment size and song characteristics for two forest bird species, an oscine passerine (orange-billed sparrow, Arremon aurantiirostris) that learns its song culturally, and a suboscine passerine (scale-crested pygmy tyrant, Lophotriccus pileatus) that does not. Recordings were taken from individuals in 12 premontane wet forest fragments ranging in size from approximately 1.4 ha–360 ha in southern Costa Rica. As predicted under the ‘cultural erosion’ hypothesis, we found that acoustic characteristics associated with song complexity such as the number of syllables per song and song duration decreased with decreasing fragment size for the oscine but not for the suboscine species. This study supports the idea that learned cultural elements are sensitive to fragment size and that cultural diversity should be considered along with other forms of biodiversity in the conservation of social learning species.

Shared territorial defence in the suboscine Aphrastura spinicauda

ABSTRACTTerritorial behaviour is an active and typically aggressive behaviour used to defend resources. Here, we investigated the presence of shared territorial defence behaviour during conspecific intrusions in the Thorn-tailed Rayadito (Aphrastura spinicauda), a suboscine species that generally does not maintain long-term pair bonds. We found that, compared to females, males displayed more alarm calling during their response, approached closer and were also more physically aggressive towards conspecific intruders. Despite these differences, the defence behaviour of males and females was highly correlated during territorial responses to simulated intruders. To our knowledge, this is the first report of coordinated or joint territorial defence in a South American suboscine that generally only maintains short-term pair bonds.

Frequency of extra-pair paternity in Scissor-tailed Flycatchers (Tyrannus forficatus) and other suboscines: are oscines and suboscines different?

ABSTRACT Extra-pair paternity (EPP) appears to be widespread in passerine birds, but few studies have focused on suboscine species, and therefore it is unclear if this generalization can be extended to this group. In this study, we document high rates of EPP in a socially monogamous, suboscine passerine, the Scissor-tailed Flycatcher (Tyrannus forficatus) in southwest Oklahoma in the summers of 2009–2011. Averaged across years, EPP occurred in 66% of nests in our study population and accounted for 49% of all nestlings. EPP rates were variable (50–88%), but did not differ significantly among years or between two study sites. Our review of the literature yielded EPP data for only 11 other species of suboscines (0.7% of total), which we compared to EPP rates for the 83 oscine species (1.9% of total) reported in Spottiswoode and Moller (2004). EPP was as common and variable in suboscines (21.7% of young) as oscines (17.5% of young). Our study adds to our knowledge of mating systems in the understudied subosci...

A putative RA-like region in the brain of the scale-backed antbird, Willisornis poecilinotus (Furnariides, Suboscines, Passeriformes, Thamnophilidae)

The memorization and production of song in songbirds share important parallels with the process of speech acquisition in humans. In songbirds, these processes are dependent on a group of specialized telencephalic nuclei known as the song system: HVC (used as a proper name), RA (robust nucleus of arcopallium), LMAN (lateral magnocellular nucleus of the nidopallium) and striatal Area X. A recent study suggested that the arcopallium of the Sayornis phoebe, a non vocal learner suboscine species, contains a nucleus with some properties similar to those of songbird RA, suggesting that the song system may have been present in the last common ancestor of these groups. Here we report morphological and gene expression evidence that a region with some properties similar to RA is present in another suboscine, the Amazonian endemic Willisornis poecilinotus. Specifically, a discrete domain with a distinct Nissl staining pattern and that expresses the RA marker RGS4 was found in the arcopallium where the oscine RA is localized. Our findings, combined with the previous report on the S. phoebe, suggest that an arcopallial region with some RA-like properties was present in the ancestor of both Suboscines infraorders Tyranni and Furnarii, and is possibly an ancestral feature of Passeriformes.

Chromosome mapping of the large elaenia (Elaenia spectabilis): evidence for a cytogenetic signature for passeriform birds?

Among birds, Tyrannidae comprises one of the most diverse and species-rich families. Although cytogenetic data have shown interesting results in this family, such as variations in the macrochromosome morphology and diploid number, only a few species have had their karyotypes described. In the present study, we report the characterization of the karyotype of Elaenia spectabilis (Passeriformes, Tyrannidae) by means of classical and molecular cytogenetics. The results show that syntenic groups of Gallus gallus (GGA) were conserved, except GGA1 and GGA4, which were divided into two different pairs each. However, the results obtained with Leucopternis albicollis probes revealed the occurrence of inversions in segments homologous to GGA1q, similar to those observed in other Passerifomes (Turdus), and one inversion in GGA1p. These results suggest that the centric fission in GGA1, as well as the inversions observed in segments homologous to GGA1q, appeared in the early history of Passeriformes because they could be detected in Oscine and Suboscine species. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115, 391–398.

Peripheral androgen action helps modulate vocal production in a suboscine passerine.

Androgenic activation of intracellular androgen receptors (AR) influences avian vocal production, though this has largely been investigated at the level of the brain. We investigated the influence of predominantly peripheral AR on vocal output in wild Golden-collared Manakins (Manacus vitellinus). In this suboscine species, males court females by performing acrobatic displays and by producing relatively simple chee-poo vocalizations. To assess whether peripheral AR influences the acoustic structure of these vocal signals, we treated reproductively active adult males with the peripherally selective antiandrogen bicalutamide and then measured phonation performance. Inhibiting AR outside of the central nervous system increased the duration of the chee note and decreased the fundamental frequency of the poo note. This treatment caused no discernable change to chee-poo frequency modulation or entropy. Our results show that activation of peripheral AR mediates note-specific changes to temporal and pitch characteristics of the Golden-collared Manakin's main sexual call. Thus, our study provides one of the first demonstrations that androgenic action originating outside of the brain and likely on musculoskeletal targets can modulate avian vocal production.

Phylogeny and classification of the New World suboscines (Aves, Passeriformes)

Here we present a phylogenetic hypothesis for the New World suboscine radiation, based on a dataset comprising of 219 terminal taxa and five nuclear molecular markers (ca. 6300 bp). We also estimate ages of the main clades in this radiation. This study corroborates many of the recent insights into the phylogenetic relationships of New World suboscines. It further clarifies a number of cases for which previous studies have been inconclusive, such as the relationships of Conopophagidae, Melanopareiidae and Tityridae. We find a remarkable difference in age of the initial divergence events in Furnariida and Tyrannida. The deepest branches in Furnariida are of Eocene age, whereas the extant lineages of Tyrannida have their origin in the Oligocene. Approximately half of the New World suboscine species are harboured in 5 large clades that started to diversify around the Mid Miocene Climatic Optimum (16-12 Mya). Based on our phylogenetic results we propose a revised classification of the New World suboscines. We also erect new family or subfamily level taxa for four small and isolated clades: Berlepschiinae, Pipritidae, Tachurididae and Muscigrallinae.

Geographical variation in the vocalizations of the suboscine Thorn‐tailed Rayadito Aphrastura spinicauda

Structural variation in acoustic signals may be related either to the factors affecting sound production such as bird morphology, or to vocal adaptations to improve sound transmission in different environments. Thus, variation in acoustic signals can influence intraspecific communication processes. This will ultimately influence divergence in allopatric populations. The study of geographical variation in vocalizations of suboscines provides an opportunity to compare acoustic signals from different populations, without additional biases caused by song learning and cultural evolution typical of oscines. The aim of this study was to compare vocalizations of distinct populations of a suboscine species, the Thorn‐tailed Rayadito. Four types of vocalizations were recorded in five populations, including all three currently accepted subspecies. Comparisons of each type of vocalization among the five populations showed that some variation existed in the repetitive trill, whereas no differences were found among alarm calls and loud trills. Variation in repetitive trills among populations and forest types suggests that sound transmission is involved in vocal differences in suboscines. Acoustic differences are also consistent with distinguishing subspecies bullocki from spinicauda and fulva, but not the two latter subspecies from each other. Our results suggest that the geographical differentiation in vocalizations observed among Thorn‐tailed Rayadito populations is likely to be a consequence of different ecological pressures. Therefore, incipient genetic isolation of these populations is suggested, based on the innate origin of suboscine vocalizations.

INDIVIDUAL VARIATION AND LEK-BASED VOCAL DISTINCTIVENESS IN SONGS OF THE SCREAMING PIHA (LIPAUGUS VOCIFERANS), A SUBOSCINE SONGBIRD

One long-standing ornithological paradigm holds that song learning in oscine songbirds has a cultural component, whereas suboscine songbirds inherit songs genetically. Recent studies reveal that suboscine song may be more variable and complex than previously realized. Several suboscine species show marked individual variation in their songs—variation that may play a role in individual recognition and neighbor–stranger discrimination—and a few suboscine species show indications of song learning. We investigated individual variation in the vocalizations of a suboscine passerine, the Screaming Piha (Lipaugus vociferans), from recordings of 26 males at four lek sites along the Tambopata River in Peru. Male Screaming Piha songs consist of quiet introductory syllables followed by two explosively loud syllables that sound like an emphatic pee haw. We used three complementary methods to examine variation in song characteristics. Spectrogram cross-correlation revealed significant consistency within individual males and variability among males. Analysis of fine structural characteristics revealed that all measured song features were significantly less variable within individuals than among individuals. Canonical discriminant analysis based on these 13 song features correctly classified 93.2% of songs by individual and 76.4% of songs by lek site. Our results indicate that there is sufficient consistency in song features within males and sufficient variation among males for identification of individuals on the basis of songs and, to a lesser extent, that song features vary with the lek site of the singer. We conclude that Screaming Pihas sing songs that are individually distinctive and bear a lek signature.

Temporal pattern of vocalization type usage in singing sessions of male tyrant flycatchers (Tyranninae)

It has been hypothesized that variation (e.g., of repertoire elements) in prolonged vocalization sessions of passerine birds can serve to minimize habituation by conspecifics. The repertoire of vocalization types limited in suboscine passerines, raising the question of how a limited set of elements can create patterns that minimize habituation. This question was studied by computational analysis of recorded singing sessions of 20 suboscine species from the subfamily Tyranninae, family Tyrannidae (tyrant flycatchers). The recordings of 12 of the species included two or more distinct vocalization types (VTs). In these species, the interval between vocalization units when the VT changed was on average shorter than that when the VT remained the same. In addition, when the VT changed, the mean interval length between successive vocalization units differed depending on which VT preceded the interval and which VT followed it. On the other hand, species with just a single VT in the session analyzed showed a surprisingly high degree of absolute difference between adjacent vocalization units with respect to both the length of the vocalization and percentage of time elapsed until peak amplitude. A change in the rhythm of vocalization accompanying a change in VT provided a potential means of drawing a conspecific listener's attention to the change in VT. The results showed that tyrant flycatchers use temporal patterning to achieve a high level of variety in vocalization sessions despite a limited vocal repertoire.

Responses of a sub-oscine bird during playback: Effects of different song variants and breeding period

Vermilion flycatchers (Pyrocephalus rubinus) vary their song rate and song length across the breeding season. Males sing more and longer songs after nest construction than before. Here we explored the possibility that this variation is meaningful to territorial males. Using a playback approach, we tested several males with different variations in song output (i.e. variations in song length and song rate) in different periods of the breeding season (i.e. before and after the onset of nest construction). We found that males call more in response to playbacks of long and short songs before the onset of nest construction. However, after nest construction began they responded flying more when exposed to long songs than to short songs. These results show that vermilion flycatcher discriminates between different variants of song length, and suggest that males react to long songs as if they were more threatening signals than short songs, especially after the onset of nest construction. We did not find evidence of males discriminating between a high and a low song rate. We discuss some possible implications for song function in this sub-oscine species, and compare these findings with other results in oscine species.

First Documentation of Combinatorial Song Syntax in a Suboscine Passerine Species

AbstractBirds with songs having two or more acoustically distinct elements can arrange them either rigidly (i.e., in the same sequence) or flexibly. Flexible song syntax can be achieved either by varying the number of repetitions of elements or by combining elements in different ways. Combinatorial syntax has been documented only in the songs of oscine passerines and in one nonpasserine, but not in the suboscine passerines. Dawn and day songs of a tyrant flycatcher, the Flammulated Attila (Attila flammulatus), were recorded in Costa Rica. Flexible syntax was noted in both dawn and day song. Attilas not only varied the number of repetitions of their song elements but also combined elements in various ways. This appears to be the first reported case of combinatorial song syntax in a suboscine species.

FIRST DOCUMENTATION OF COMBINATORIAL SONG SYNTAX IN A SUBOSCINE PASSERINE SPECIES

Birds with songs having two or more acoustically distinct elements can arrange them either rigidly (i.e., in the same sequence) or flexibly. Flexible song syntax can be achieved either by varying the number of repetitions of elements or by combining elements in different ways. Combinatorial syntax has been documented only in the songs of oscine passerines and in one nonpasserine, but not in the suboscine passerines. Dawn and day songs of a tyrant flycatcher, the Flammulated Attila (Attila flammulatus), were recorded in Costa Rica. Flexible syntax was noted in both dawn and day song. Attilas not only varied the number of repetitions of their song elements but also combined elements in various ways. This appears to be the first reported case of combinatorial song syntax in a suboscine species.

Estrogen receptors in the avian brain: Survey reveals general distribution and forebrain areas unique to songbirds

Estrogens play an important role in the control and differentiation of species-typical behavior and in endocrine homeostasis of birds, but the distribution and evolution of cells that contain estrogen receptors in the avian brain are poorly understood. This study therefore surveys 26 species in the avian orders Anseriformes (1 species), Galliformes (2), Columbiformes (3), Psittaciformes (1), Apodiformes (2), and Passeriformes (3 suboscines, 14 oscines). Indirect immunocytochemistry with the estrogen receptor (ER) antibody H222Spy revealed a general pattern of ER-antibody-immunoreactive cells (ER-IRC) in all 26 species, with ER-IRC in consistent, well-defined locations in the limbic forebrain, the midbrain striatum, the hippocampus, the hindbrain, and especially in the preoptic area and the tuberal hypothalamus. For some species, the microdistribution of ER-IRC in some of these general areas differed, such as in the hippocampus and the anterior hypothalamus of suboscine species and in the preoptic area of the Japanese quail. Brains of oscine songbirds of both sexes, unlike brains of nonsongbirds, had ER-IRC in three specific structures of the nonlimbic forebrain: in the area surrounding the nucleus robustus archistriatalis; in the rostral forebrain; and, for all individuals, in the caudale neostriatum, including the nucleus hyperstriatalis ventrale, pars caudale (HVc). Among songbird families or subfamilies, adult males of the Estrildinae had much lower numbers of ER-IRC in HVc than did adult males of the Fringillidae, Paridae, Sturnidae, and Ploceinae. Differences occurred, too, among closely related species: the songbird canary (Serinus canaria) had an ER-IRC area in the rostral forebrain that was lacking in all other songbird species, including other cardueline finches. The cells with ER that are found only in the songbird forebrain but not in reptiles, nonpasserine birds, and nonoscine passerine birds very likely coevolved with steroid-dependent differentiation of vocal control areas. The songbird-specific expression of ER in the forebrain could be an example in which taxon-specific behavior is due to taxon specific neurochemical properties of the brain.