Paridae Species Research Articles

Unlearned adaptive responses to heterospecific referential alarm calls in two bird species from separate evolutionary lineages

The interspecific responses to alarm signals may be based on unlearned mechanisms but research is often constrained by the difficulties in differentiating between unlearned and learned responses in natural situations. In a field study of two Paridae species, Parus minor and Sittiparus varius, who originated from a common ancestor 8 million years ago, we found a considerable degree of between-species overlap in acoustic properties of referential snake-alarm calls. Playback of these calls triggered unlearned adaptive fledging behavior in conspecific and heterospecific naive nestlings, suggesting a between-species overlap in the hypothetical unlearned neural templates involved in nestlings’ reactions to alarm calls in both species. This suggests that similar calls and similar unlearned sensitivity might have been present in the common ancestor of the two species, and possibly in the ancestor of the whole family Paridae that originated 10–15 million years ago in Asian regions rich in snakes.

The phenology and clutch size of UK Blue Tits does not differ with woodland composition

The deciduous tree‐herbivorous caterpillar‐insectivorous bird food chain is a well‐studied system for investigating the impacts of climate change across trophic levels. To date, across Europe, most attention has focused on the impacts of increasing spring temperature on changes to phenology in Oak‐dominated (Quercus spp.) woodlands. Paridae species and Pied Flycatcher Ficedula hypoleuca are the most studied secondary consumers, all of which demonstrate an advancement in reproductive phenology with increases in spring temperature. Shifts in climate and phenology may also impact on reproductive investment in clutch size, and the effects of climate on phenology and clutch size may vary depending on woodland composition. To date, the effects of among‐habitat variation in phenology and reproductive investment have received little attention. Insectivorous birds inhabiting woodlands that differ in tree composition may differ in the timing of breeding, due to local tree leafing phenology acting as a cue for egg‐laying date and/or clutch size. Moreover, for most insectivorous birds, woodland composition within a territory is likely to be the main determinant of food availability for both adults and chicks. Consequently, if warming springs affect the temporal patterns of food availability differently across different woodland compositions, this may affect the optimal average local phenology for nesting birds. Here, using data from 34 long‐term (mean 15 years) nest monitoring sites across the UK, we investigate the effect of woodland tree composition and temperature on Blue Tit Cyanistes caeruleus first egg date (FED) and clutch size. We supplemented the nest monitoring data by quantifying woodland composition, at a site level, through modified point counts. We predict that birds breeding in woodlands with greater proportions of late‐leafing species, such as Oak and Ash Fraxinus excelsior, will breed later than those breeding in woodlands with greater proportions of early‐leafing species, such as Birch Betula spp. and Beech Fagus sylvatica. We found no evidence for differences in Blue Tit FED or clutch size in relation to the proportion of any of the tree species investigated, after controlling for temperature and latitude (FED: −3.4 and 2.2, clutch size: −0.4 and − 0.2 eggs for one‐unit increase in temperature and latitude, respectively). In recent decades and across all sites, clutch size has decreased as spring temperatures have increased, a strategy which could allow birds flexibly to adjust their breeding phenology such that nestling demand coincides with peak food availability. The lack of an effect of woodland composition on Blue Tit phenology suggests Blue Tits do not fine‐tune their reproductive phenology to the local tree composition. Whether this lack of evidence for phenological divergence is due to an absence of divergent selection on breeding phenology and clutch size or to gene flow is not clear.

A community context for aggression? Multi-species audience effects on territorial aggression in two species of Paridae.

Territorial aggression in birds is widely observed and is commonly linked to sex, age, body size, physiology, seasonal cues, food resource, urbanization, and a variety of social contexts including conspecific audience effects. However, little is known about the heterospecific audience effects on territorial aggression.Here, we address an emerging idea that heterospecific audience effects may be pervasive influences in the social lives of free‐living birds. We tested the hypothesis that the composition, number, and relative body size of heterospecific audiences observing an aggressive contest will influence the response probability and intensity of aggression displayed.We subjected two Paridae species, tufted titmouse (TUTI, Baeolophus bicolor) and Carolina chickadee (CACH, Poecile carolinensis), to playbacks of aggressive calls during a breeding season in north‐central Florida. At widely spaced playback sites (N = 134) in woodland habitats, we characterized the makeup of heterospecific audiences, aggression type (intra vs. interspecific territoriality), local population density, and various environmental factors (tree density, wind speed, and noise level) that are likely to influence territorial aggression.We found that the presence of heterospecific audiences increased TUTI aggression levels and that both parids were more likely to respond to playback stimuli when their audiences had higher heterospecific diversity (more heterospecific individuals and species). We also found TUTI were more likely to respond when CACH were present but not vice versa.In conclusion, we found evidence that heterospecific audiences significantly influenced the metrics of territorial aggression of free‐living animals and we suggest that the definition of audience effects on the behavior of free‐living animals be expanded to incorporate heterospecific audiences.

Habitat preferences of Sombre Tit (Poecile lugubris) in a karst environment

Sombre Tit (Poecile lugubris) is one of the least studied passerine bird species in Europe, and the least known among Paridae species on the continent. The aim of the study is to identify its habitat preferences in a karst environment. The study took place in 2016–2017 within the “Rayanovtsi” Special Protection Area in Western Bulgaria – a limestone terrain with a mosaic of open areas, shrubs and scattered woodland, featured by sinkholes, rocks and caves. Territory and control plots were identified by means of point counts and territory mapping. To quantitatively describe the habitat structure and the fine-scale land-cover, 17 habitat variables were measured at both territory and control plots (the latter located at unoccupied sites), within a radius (180 m) approximating the territory size of the species.

Great tit responses to the calls of an unfamiliar species suggest conserved perception of call ordering

Many species of birds produce distinct calls when mobbing predators. These calls often recruit nearby conspecifics and heterospecifics to help drive the predators away. In some species, such as members of the family Paridae, mobbing calls are composed of multiple elements that seem to follow a characteristic order. Previous work in parids demonstrated that note ordering influences both the responses of conspecifics and some other co-occurring Paridae species. Cross-species sensitivity to note ordering could result from individuals’ learning to associate individual heterospecific calls with threats or, rather, because the typical note orderings are shared across species. Here, we test these hypotheses by assessing the responses of European great tits (Parus major) to the naturally and artificially ordered calls of black-capped chickadees (Poecile atricapillus), a North American species. In response to the naturally ordered mobbing calls of chickadees, we found that great tits exhibit vigilance and rapidly approach the sound source, behaviors that were indistinguishable to those expressed in response to conspecific calls. If learned associations are necessary for sensitivity to note ordering, then a key prediction is that great tit responses to naturally ordered and artificially reversed chickadee calls should be similar (and weak). In contrast to this prediction, we found that great tits were less vigilant, but approach the sound source in response to artificially reversed chickadee calls. These findings suggest that perception of note ordering patterns is conserved. However, they are also in agreement with a “perception bias” hypothesis: that the first notes of the call mask the notes that follow them, preventing the receiver from perceiving the second part of the call. Although we provide evidence against perception bias, further research is needed to convincingly disentangle these two hypotheses. How do animals decode other species’ vocal sequences? Great tit responses to chickadee sequences depend on the ordering of their notes. Great tits and chickadees never encounter one another in the wild, but their alarm call sequences have similar note orderings. Using a series of playback experiments, we demonstrate that great tits respond strongest to chickadee calls whose order matches their own. Thus, response to unfamiliar calls does not depend on learning, but, rather, shared call ordering across species.

Phylogenetic relationship and characterization of the complete chloroplast genome of the alpine leaf-warbler in Qinghai-Tibet Plateau

The Alpine Leaf-warbler (Phylloscopus occisinensis) is a small-sized and poorly-known songbird endemic to China. In this study, we sequenced and described the whole mitochondrial genome of the Alpine leaf-warbler. The entire mitochondrial sequence was determined by long-range PCR and conserved primer walking approaches. The results demonstrated that the whole mitochondrial genome of P. occisinensis was 16,879 bp in length with 53.1% A + T content; the genome harboured the same gene order as that of other passerine birds, including 13 protein-coding genes, 2 rRNA genes, 22 tRNA genes and non-coding control region. The control region (D-loop) of P. rubicilloides include two portions that one was located between tRNA-Gln and tRNA-Phe (219 bp in length) and the other is between tRNA-Thr and tRNA- Pro (1087 bp in length), which is similar to other Leaf-warblers. Phylogenetic analysis indicated that the genome of Phylloscopus species clustered within a clade and is closer related to Aegithalidae species than Paridae species. These mitochondrial data are potentially important for the further studies on molecular evolution and conservation genetics on leaf warbler species.

Subtle variations in mobbing calls are predator-specific in great tits (Parus major)

Many species are known to use vocalizations to recruit con- and heterospecifics to mobbing events. In birds, the vocalizations of the Family Paridae (titmice, tits and chickadees) are well-studied and have been shown to recruit conspecifics and encode information about predation risk. Species use the number of elements within a call, call frequency or call type to encode information. We conducted a study with great tits (Parus major) in the field where we presented taxidermy mounts of two predators of different threat levels (tawny owl, Strix aluco, and sparrowhawk, Accipiter nisus) and compared the mobbing calls of these two contexts. We hypothesized, based on results of studies in other paridae species, that tits vary the number or type of elements of a call according to predatory context. We found great tits to vary the number of D elements and the interval between those elements. Great tits produced significantly longer D calls with more elements and longer intervals between elements when confronted with a sparrowhawk (high-threat) compared to a tawny owl (low-threat) mount. Furthermore, birds produced more D calls towards the high-threat predator. This suggests that the basic D calls are varied depending on threat intensity.

Breeding Biology of Four Sympatric Tits In Northern Japan

ABSTRACT In order to understand evolution in life history strategies, it is useful to compare breeding parameters among closely related species and/or different habitats within the same species. The Paridae family, known as tits and chickadees, are suitable for such studies since they are distributed worldwide and use a variety of habitats. However, previous studies are mostly limited to populations in Europe and North America. Few studies have compared breeding biology in sympatric Paridae species. In this study, we investigated the breeding biology of Japanese Tits (Parus minor), Coal Tits (Periparus ater), Marsh Tits (Poecile palustris), and Varied Tits (Sittiparus varius) in a cool temperate forest of northern Japan. A previous study has shown that Japanese Tits have higher annual production (i.e., clutch size, rate of multiple brooding) compared to a European sister species, the Great Tit (Parus major), possibly because of greater diversity and abundance of prey items. Therefore, we predicted that an...

Nested PCR for Suttonella ornithocola reveals widespread infection in British Paridae species

Suttonella ornithocola, a bacterium in the Cardiobacteriaceae family, is postulated to act as a pathogen targeting the respiratory tract of wild birds in the tit families (Paridae and Aegithalidae). This organism has fastidious culture requirements, which might lead to missed detection; thus, a nested PCR targeting the 16S rRNA gene was designed to provide an additional detection tool. DNA was extracted from combined lung and trachea samples from 114 birds in the Paridae and five in the Aegithalidae. These wild birds were found dead across England and Wales, 2005–2012 inclusive, and examined post-mortem. The PCR detected S. ornithocola in 15 birds from the Paridae family only: 11 blue tits (Cyanistes caeruleus), three great tits (Parus major) and one coal tit (Periparus ater). Derived sequences of the 16S rRNA gene had 100% identity to S. ornithocola from previous studies. Positive cases had a widespread geographical distribution across the study period with recurrent spring seasonality, consistent with an endemic infection. Incident history and pathological findings indicated that S. ornithocola infection was likely to be a significant contributory factor to the deaths of at least two birds (from two sites), was of equivocal significance in four birds (from four sites) and was an incidental finding in nine birds (from eight sites). Nested PCR detected S. ornithocola in ten birds for which microbiological examination of the lung was culture-negative for the bacterium. A combination of molecular, microbiological and histopathological examinations is recommended to further investigate the epidemiology and significance of S. ornithocola infection.

A comparative study of how British tits encode predator threat in their mobbing calls

Many species use antipredator vocalizations to signal information about potential predators, including the level of threat posed by a particular predator. It is not clear, however, why only some prey species do this. Because they use multiple mechanisms to encode threat-specific information about predators, North American Paridae species have been a particularly useful model for studying antipredator signals. Paridae as a group are also useful for examining phylogenetic conservation of vocal signals because all of these species (at least those studied previously) employ similar ways of encoding information about predator threat. To test whether the ways in which predator threat information is encoded (here measured by a bird's vocal output) are conserved across a family with similar vocalizations, we used taxidermy mounts to simulate low- and high-threat predators to induce mobbing in six species across five genera of British Paridae. We found that, like North American species, British tits all increased their call rate in response to predators compared with nonthreatening control mounts, but they all varied in the number and types of additional ways they encoded this information. Some species (blue and willow tits) used all four ways to differentiate between different threat predators, while others used only two (crested tits), one (great and coal tits) or none at all (willow tits). The variation in the way each species encoded predator threat information in their calls was not explained by phylogenetic relatedness or by variation in life history. To better understand patterns of information encoding across related species, we suggest that playback experiments to determine how encoded information is used by conspecifics and heterospecifics might provide insights about why some species encode information about predator threat in multiple ways.

Evolution of body morphology and beak shape revealed by a morphometric analysis of 14 Paridae species.

BackgroundMorphological characters of birds reflect their adaptive evolution and ecological requirements and are also relevant to phylogenetic relationships within a group of related species. The tits (Paridae) are known to be outwardly homogeneous in shape, with one aberrant member, the Ground Tit (Pseudopodoces humilis), which is quite different from its relatives in both body morphology and beak shape. We combined traditional measurements and geometric morphometrics to quantify the variation in body morphology and beak shape of 14 Paridae species distributed in China. Based on these results, we sought to assess the contribution of phylogeny, altitude and species interactions to the evolution of morphological traits.ResultsThe basic features for discriminating among the 14 species studied here were overall body size, the ratio of body and tail length to culmen and tarsus length, and beak shape (long/slender/pointy vs. short/robust/blunt). These dimensions clearly separate Ps. humilis and Melanochlora sultanea from the other species in shape space. Body length and PC3 of beak shape (round outline vs. straight outline) show significant phylogenetic signals. Across 14 species, altitude is related to tarsus, culmen length and PC1 of beak shape. Within Parus major, altitude is related to body weight, body length, culmen length and PC1 of body morphology. Morphological distances and geographic distances among species are positively correlated.ConclusionsThe body morphology of Paridae species shows extensive evolutionary changes, while their beak has mainly evolved along the long/slender/pointy vs. short/robust/blunt dimension. Only body length and beak curvature show a phylogenetic signal. Altitude correlates with multiple traits both across and within species, suggesting that altitude is an important factor in promoting morphological divergence. The deviant appearance of Ps. humilis corresponds to its foraging and feeding adaptations to high-altitude steppe habitats. Our results also show a higher level of morphological divergence with greater difference in distribution ranges among the Paridae species involved in this study.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-016-0162-0) contains supplementary material, which is available to authorized users.

Fine-scale characterization of bird habitat using airborne LiDAR in an urban park in Japan

Birds are ecosystem service providers and excellent urban ecosystem indicators because they are sensitive to habitat structure. Light detection and ranging (LiDAR) technology is a promising tool in bird habitat characterization because it can directly acquire fine-scale 3-D information over large areas; however, most of past avian ecological studies using LiDAR were conducted in North America and Europe, and there have been no studies in Asia. The robustness of LiDAR data across different habitat types remain problematic. In this study, we set 13 plots having different canopy area percentages in a large-scale urban park in Japan, and examined the usefulness of airborne LiDAR data in modeling richness and diversity of forest bird species and the abundance of Paridae species that play an important role in the urban food web. Bird surveys were conducted eight times at each plot during the birds’ breeding season, and the results were estimated using generalized linear models. In consequence, all of the response variables were explained by one or a few LiDAR variables, and the 1×1×1-m voxel-based variables were especially robust estimators. When targeting only densely-forested plots having more than 60% canopy area, the LiDAR data efficiency declined in estimation of the richness and diversity of whole forest bird species, whereas a laser penetration rate was efficient for estimating the Paridae species abundance. These results implied that the LiDAR data are useful in habitat characterization of forest birds, and even when targeting only dense forests, some LiDAR variables are effective for habitat estimation of birds preferring specific forest structures. In the future, application of LiDAR across a variety of ecosystems will greatly serve to develop adaptive conservation and management planning for urban forests.

Epidemiology of the emergent disease Paridae pox in an intensively studied wild bird population.

Paridae pox, a novel avipoxvirus infection, has recently been identified as an emerging infectious disease affecting wild tit species in Great Britain. The incursion of Paridae pox to a long-term study site where populations of wild tits have been monitored in detail for several decades provided a unique opportunity to obtain information on the local-scale epidemiological characteristics of this novel infection during a disease outbreak. Using captures of >8000 individual birds, we show that, within two years of initial emergence, Paridae pox had become established within the population of great tits (Parus major) reaching relatively high peak prevalence (10%), but was far less prevalent (<1%) in sympatric populations of several other closely related, abundant Paridae species. Nonlinear smoothing models revealed that the temporal pattern of prevalence among great tits was characterised by within-year fluctuations indicative of seasonal forcing of infection rates, which was likely driven by multiple environmental and demographic factors. There was individual heterogeneity in the course of infection and, although recovery was possible, diseased individuals were far less likely to be recaptured than healthy individuals, suggesting a survival cost of infection. This study demonstrates the value of long-term monitoring for obtaining key epidemiological data necessary to understand disease dynamics, spread and persistence in natural populations.

Information theoretical approaches to chick-a-dee calls of Carolina chickadees (Poecile carolinensis).

One aim of this study was to apply information theoretical analyses to understanding the structural complexity of chick-a-dee calls of Carolina chickadees, Poecile carolinensis. A second aim of this study was to compare this structural complexity to that of the calls of black-capped chickadees, P. atricapillus, described in an earlier published report (Hailman, Ficken, & Ficken, 1985). Chick-a-dee calls were recorded from Carolina chickadees in a naturalistic observation study in eastern Tennessee. Calls were analyzed using approaches from information theory, including transition probability matrices, Zipf's rules, entropies, and information coding capacities of calls and notes of calls. As described for black-capped chickadees, calls of Carolina chickadees exhibited considerable structural complexity. Most results suggested that the call of Carolina chickadees is more structurally complex than that of black-capped chickadees. These findings add support to the growing literature on the complexity of this call system in Paridae species. Furthermore, these results point to the feasibility of detailed cross-species comparative analyses that may allow strong testing of hypotheses regarding signal evolution.

Why some tits store food and others do not: evaluation of ecological factors

Paridae are among the bird families benefiting from food storing. However, not all its members hoard food. Our objective was to clarify the role of ecological factors in occurrence of food storing. We reviewed the data on major ecological characteristics of the Paridae species and analysed their association with the presence/absence of food storing. Our statistical model revealed that geography (distribution in North America) and taxonomy (genus Poecile) are better predictors of food storing than any of the studied ecological traits. Nevertheless, food-storing Poecile species inhabit mixed or coniferous woodlands with seasonal richness of food, while non-storing species tend to prefer edge and open habitats, where alternative food sources are available. Sociality and territoriality outside breeding season coincides with food storing. The analysis performed within the Baeolophus–Lophophanes–Periparus–Poecile clade with ancestral food storing revealed no factor except continental climate that would explain the persistence of food storing. The phylogenetic analysis of ancestral states of the studied characters allowed us to propose a possible scenario for the emergence of food storing in Paridae. (1) Food storing is not ancestral in Paridae and appeared only once in the common ancestor of the Baeolophus–Lophophanes–Periparus–Poecile group. (2) According to estimation of molecular clock in Paridae, food storing appeared before their radiation in North America.

Chick-a-dee call variation in Carolina chickadees and recruiting flockmates to food

The “chick-a-dee” call of many Paridae species (titmice, tits, and chickadees) is structurally complex and functions in social cohesion. Studies with different Parid species suggest that variation in the note composition of calls relates to a wide variety of contexts. An earlier study with Carolina chickadees (Poecile carolinensis), the focal species of the present study, found that receivers responded differently to playback calls differing in note composition in feeding contexts. Here, we addressed whether signalers actually produce calls differing in note composition in feeding contexts and whether those calls might serve a recruitment function. In a first study, we found that the first chickadee to take seed from a feeding station produced calls with a greater number of D notes before the second chickadee arrived to take seed, compared with after the second chickadee arrived to take seed. This suggests that calls with a large number of D notes might serve a general recruitment function. We tested this idea in a second study, using playbacks of calls containing a large number of D notes or a small number of D notes at different sites. We found that the latency for a first chickadee to come into a site and take seed was shorter for playback variants containing a large number of D notes. Thus, in Carolina chickadees, chick-a-dee calls containing a large number of D notes may function to recruit other flock members to a discovered food source.