Inhibitory network interactions shape the auditory processing of natural communication signals in the songbird auditory forebrain

The role of GABA in the central processing of complex auditory signals is not fully understood. We have studied the involvement of GABA(A)-mediated inhibition in the processing of birdsong, a learned vocal communication signal requiring intact hearing for its development and maintenance. We focused on caudomedial nidopallium (NCM), an area analogous to parts of the mammalian auditory cortex with selective responses to birdsong. We present evidence that GABA(A)-mediated inhibition plays a pronounced role in NCM`s auditory processing of birdsong. Using immunocytochemistry, we show that approximately half of NCM`s neurons are GABAergic. Whole cell patch-clamp recordings in a slice preparation demonstrate that, at rest, spontaneously active GABAergic synapses inhibit excitatory inputs onto NCM neurons via GABA(A) receptors. Multi-electrode electrophysiological recordings in awake birds show that local blockade of GABA(A)-mediated inhibition in NCM markedly affects the temporal pattern of song-evoked responses in NCM without modifications in frequency tuning. Surprisingly, this blockade increases the phasic and largely suppresses the tonic response component, reflecting dynamic relationships of inhibitory networks that could include disinhibition. Thus processing of learned natural communication sounds in songbirds, and possibly other vocal learners, may depend on complex interactions of inhibitory networks.

Spatial Aggregation of Forest Songbird Territories and Possible Implications for Area Sensitivity

Habitat area requirements of forest songbirds vary greatly among species, but the causes of this variation are not well understood. Large area requirements could result from advantages for certain species when settling their territories near those of conspecifics. This phenomenon would result in spatial aggregations much larger than single territories. Species that aggregate their territories could show reduced population viability in highly fragmented forests, since remnant patches may remain unoccupied if they are too small to accommodate several territories. The objectives of this study were twofold: (1) to seek evidence of territory clusters of forest birds at various spatial scales, lags of 250-550 m, before and after controlling for habitat spatial patterns; and (2) to measure the relationship between spatial autocorrelation and apparent landscape sensitivity for these species. In analyses that ignored spatial variation of vegetation within remnant forest patches, nine of the 17 species studied significantly aggregated their territories within patches. After controlling for forest vegetation, the locations of eight out of 17 species remained significantly clustered. The aggregative pattern that we observed may, thus, be indicative of a widespread phenomenon in songbird populations. Furthermore, there was a tendency for species associated with higher forest cover to be more spatially aggregated [ERRATUM].

Forest Policy Scenario Analysis: Sensitivity of Songbird Community to Changes in Forest Cover Amount and Configuration

Changes in mature forest cover amount, composition, and configuration can be of significant consequence to wildlife populations. The response of wildlife to forest patterns is of concern to forest managers because it lies at the heart of such competing approaches to forest planning as aggregated vs. dispersed harvest block layouts. In this study, we developed a species assessment framework to evaluate the outcomes of forest management scenarios on biodiversity conservation objectives. Scenarios were assessed in the context of a broad range of forest structures and patterns that would be expected to occur under natural disturbance and succession processes. Spatial habitat models were used to predict the effects of varying degrees of mature forest cover amount, composition, and configuration on habitat occupancy for a set of 13 focal songbird species. We used a spatially explicit harvest scheduling program to model forest management options and simulate future forest conditions resulting from alternative forest management scenarios, and used a process-based fire-simulation model to simulate future forest conditions resulting from natural wildfire disturbance. Spatial pattern signatures were derived for both habitat occupancy and forest conditions, and these were placed in the context of the simulated range of natural variation. Strategic policy analyses were set in the context of current Ontario forest management policies. This included use of sequential time-restricted harvest blocks (created for Woodland caribou (Rangifer tarandus) conservation) and delayed harvest areas (created for American marten (Martes americana atrata) conservation). This approach increased the realism of the analysis, but reduced the generality of interpretations. We found that forest management options that create linear strips of old forest deviate the most from simulated natural patterns, and had the greatest negative effects on habitat occupancy, whereas policy options that specify deferment and timing of harvest for large blocks helped ensure the stable presence of an intact mature forest matrix over time. The management scenario that focused on maintaining compositional targets best supported biodiversity objectives by providing the composition patterns required by the 13 focal species, but this scenario may be improved by adding some broad-scale spatial objectives to better maintain large blocks of interior forest habitat through time.

The Importance of Agriculture-Dominated Landscapes and Lack of Field Border Effect for Early-Succession Songbird Nest Success

In recent decades, many early-succession songbird species have experienced severe and widespread declines, which often are related to habitat destruction. Field borders create additional or enhance existing early-succession habitat on farmland. However, field border shape and the landscape context surrounding farms may influence the effectiveness of field borders in contributing to the stabilization or increase of early-succession bird populations. We examined the influence of linear and nonlinear field borders on farms in landscapes dominated by either agriculture or forests on nest success and Brown-headed Cowbird (Molothrus ater) brood parasitism of Indigo Bunting (Passerina cyanea) and Blue Grosbeak (Passerina caerulea) nests combined. Field border establishment did not affect nest survival probability and brood parasitism frequency of Indigo Bunting and Blue Grosbeak nests. Indigo Bunting/Blue Grosbeak nest success probability was more than twice as high in agriculture-dominated landscapes (39%) than in forested landscapes (17%), and brood parasitism frequency was high (33%) but did not differ between landscapes. Edges in agriculture-dominated landscapes can be higher-quality habitats for early-succession birds than edges in forest-dominated landscapes, but our field border treatments did not enhance nest success for these birds on farms in either landscape.

How well do regional or national Breeding Bird Survey data predict songbird population trends at an intact boreal site?

A study to monitor boreal songbird trends was initiated in 1998 in a relatively undisturbed and remote part of the boreal forest in the Northwest Territories, Canada. Eight years of point count data were collected over the 14 years of the study, 1998-2011. Trends were estimated for 50 bird species using generalized linear mixed-effects models, with random effects to account for temporal (repeat sampling within years) and spatial (stations within stands) autocorrelation and variability associated with multiple observers. We tested whether regional and national Breeding Bird Survey (BBS) trends could, on average, predict trends in our study area. Significant increases in our study area outnumbered decreases by 12 species to 6, an opposite pattern compared to Alberta (6 versus 15, respectively) and Canada (9 versus 20). Twenty-two species with relatively precise trend estimates (precision to detect > 30% decline in 10 years; observed SE ≤ 3.7%/year) showed nonsignificant trends, similar to Alberta (24) and Canada (20). Precision-weighted trends for a sample of 19 species with both reliable trends at our site and small portions of their range covered by BBS in Canada were, on average, more negative for Alberta (1.34% per year lower) and for Canada (1.15% per year lower) relative to Fort Liard, though 95% credible intervals still contained zero. We suggest that part of the differences could be attributable to local resource pulses (insect outbreak). However, we also suggest that the tendency for BBS route coverage to disproportionately sample more southerly, developed areas in the boreal forest could result in BBS trends that are not representative of range-wide trends for species whose range is centred farther north.

Immigration, species radiation and extinction in a highly diverse songbird lineage: white-eyes on Indian Ocean islands

Molecular phylogenetic hypotheses of species-rich lineages in regions where geological history can be reliably inferred may provide insights into the scale of processes driving diversification. Here we sample all extant or recently extinct white-eye (Zosterops) taxa of the southwest Indian Ocean, combined with samples from all principal continental lineages. Results support a high dispersal capability, with at least two independent continental sources for white-eyes of the region. An early (within 1.8 million years ago) expansion into the Indian Ocean may have originated either from Asia or Africa; the three resulting lineages show a disparate distribution consistent with considerable extinction following their arrival. Africa is supported as the origin of a later expansion into the region (within 1.2 million years ago). On two islands, a pair of Zosterops species derived from independent immigrations into the Indian Ocean co-occur or may have formerly co-occurred, providing strong support for their origin by double-island colonization rather than within-island (sympatric or microallopatric) speciation. On Mauritius and La Reunion, phylogenetic placement of sympatric white-eyes allow us to rule out a scenario in which independent within-island speciation occurred on both islands; one of the species pairs must have arisen by double colonization, while the other pair is likely to have arisen by the same mechanism. Long-distance immigration therefore appears to be responsible for much of the region's white-eye diversity. Independent immigrations into the region have resulted in lineages with mutually exclusive distributions and it seems likely that competition with congeneric species, rather than arrival frequency, may limit present-day diversity.

Mechanisms underlying the sensitivity of songbird forebrain neurons to temporal order.

Neurons in the songbird forebrain area HVc (hyperstriatum ventrale pars caudale or high vocal center) are sensitive to the temporal structure of the bird's own song and are capable of integrating auditory information over a period of several hundred milliseconds. Extracellular studies have shown that the responses of some HVc neurons depend on the combination and temporal order of syllables from the bird's own song, but little is known about the mechanisms underlying these response properties. To investigate these mechanisms, we recorded intracellular responses to a set of auditory stimuli designed to assess the degree of dependence of the responses on temporal context. This report provides evidence that HVc neurons encode information about temporal structure by using a variety of mechanisms including syllable-specific inhibition, excitatory postsynaptic potentials with a range of different time courses, and burst-firing nonlinearity. The data suggest that the sensitivity of HVc neurons to temporal combinations of syllables results from the interactions of several cells and does not arise in a single step from afferent inputs alone.

Decrements in auditory responses to a repeated conspecific song are long-lasting and require two periods of protein synthesis in the songbird forebrain.

Earlier work showed that playbacks of conspecific song induce expression of the immediate early gene ZENK in the caudo-medial neostriatum (NCM) of awake male zebra finches and that this response disappears with repeated presentations of the same stimulus. In the present study, we investigated whether repetitions of a song stimulus also elicited a decrement in the electrophysiological responses in the NCM neurons of these birds. Multiunit auditory responses in NCM were initially vigorous, but their amplitude decreased (habituated) rapidly to repeated stimulation, declining to about 40% of the initial response during the first 50 iterations. A similar time course of change was seen at the single unit level. This habituation occurred specifically for each song presented but did not occur when pure tones were used as a stimulus. Habituation to conspecific, but not heterospecific, song was retained for 20 h or longer. Injections of inhibitors of protein or RNA synthesis at the recording site did not affect the initial habituation to a novel stimulus, but these drugs blocked the long-term habituation when injected at 0.5-3 h and at 5.5-7 h after the first exposure to the stimulus. Thus, at least two waves of gene induction appear to be necessary for long-lasting habituation to a particular song.

Factors driving territory size and breeding success in a threatened migratory songbird, the Canada Warbler

Successful conservation of migratory birds demands we understand how habitat factors on the breeding grounds influences breeding success. Multiple factors are known to directly influence breeding success in territorial songbirds. For example, greater food availability and fewer predators can have direct effects on breeding success. However, many of these same habitat factors can also result in higher conspecific density that may ultimately reduce breeding success through density dependence. In this case, there is a negative indirect effect of habitat on breeding success through its effects on conspecific density and territory size. Therefore, a key uncertainty facing land managers is whether important habitat attributes directly influence breeding success or indirectly influence breeding success through territory size. We used radio-telemetry, point-counts, vegetation sampling, predator observations, and insect sampling over two years to provide data on habitat selection of a steeply declining songbird species, the Canada Warbler (Cardellina canadensis). These data were then applied in a hierarchical path modeling framework and an AIC model selection approach to determine the habitat attributes that best predict breeding success. Canada Warblers had smaller territories in areas with high shrub cover, in the presence of red squirrels (Tamiasciurus hudsonicus), at shoreline sites relative to forest-interior sites and as conspecific density increased. Breeding success was lower for birds with smaller territories, which suggests competition for limited food resources, but there was no direct evidence that food availability influenced territory size or breeding success. The negative relationship between shrub cover and territory size in our study may arise because these specific habitat conditions are spatially heterogeneous, whereby individuals pack into patches of preferred breeding habitat scattered throughout the landscape, resulting in reduced territory size and an associated reduction in resource availability per territory. Our results therefore highlight the importance of considering direct and indirect effects for Canada warblers; efforts to increase the amount of breeding habitat may ultimately result in lower breeding success if habitat availability is limited and negative density dependent effects occur.

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Understanding Demographic and Behavioral Mechanisms that Guide Responses of Neotropical Migratory Birds to Urbanization: a Simulation Approach

Although studies often report that densities of many forest birds are negatively related to urbanization, the mechanisms guiding this pattern are poorly understood. Our objective was to use a population simulation to examine the relative influence of six demographic and behavioral processes on patterns of avian abundance in urbanizing landscapes. We constructed an individual-based population simulation model representing the annual cycle of a Neotropical migratory songbird. Each simulation was performed under two landscape scenarios. The first scenario had similar proportions of high- and low-quality habitat across the urban to rural gradient. Under the first scenario, avian density was negatively related to urbanization only when rural habitats were perceived to be of higher quality than they actually were. The second landscape scenario had declining proportions of high-quality habitat as urbanization increased. Under the second scenario, each mechanism generated a negative relationship between density and urbanization. The strongest effect on density resulted when birds preferentially selected habitats in landscapes from which they fledged or were constrained from dispersing. The next strongest patterns occurred when birds directly evaluated habitat quality and accurately selected the highest-quality available territories. When birds selected habitats based on the presence of conspecifics, the density–urbanization relationship was only one-third the strength of other habitat selection mechanisms and only occurred under certain levels of population survival. Although differences in adult or nest survival in the face of random habitat selection still elicited reduced densities in urban landscapes, the relationships between urbanization and density were weaker than those produced by the conspecific attraction mechanism. Results from our study identify key predictions and areas for future research, including assessing habitat quality in urban and rural areas in order to determine if habitats in urban areas are underutilized.