The evolution of the avian bill as a thermoregulatory organ.

The avian bill is a textbook example of how evolution shapes morphology in response to changing environments. Bills of seed-specialist finches in particular have been the focus of intense study demonstrating how climatic fluctuations acting on food availability drive bill size and shape. The avian bill also plays an important but under-appreciated role in body temperature regulation, and therefore in energetics. Birds are endothermic and rely on numerous mechanisms for balancing internal heat production with biophysical constraints of the environment. The bill is highly vascularised and heat exchange with the environment can vary substantially, ranging from around 2% to as high as 400% of basal heat production in certain species. This heat exchange may impact how birds respond to heat stress, substitute for evaporative water loss at elevated temperatures or environments of altered water availability, or be an energetic liability at low environmental temperatures. As a result, in numerous taxa, there is evidence for a positive association between bill size and environmental temperatures, both within and among species. Therefore, bill size is both developmentally flexible and evolutionarily adaptive in response to temperature. Understanding the evolution of variation in bill size however, requires explanations of all potential mechanisms. The purpose of this review, therefore, is to promote a greater understanding of the role of temperature on shaping bill size over spatial gradients as well as developmental, seasonal, and evolutionary timescales.

Avian responses to an emergent, wetland weed

African boxthorn (Lycium ferocissimum Solanaceae) is a Weed of National Significance in Australia. It is particularly problematic in Victoria and is thought to not only threaten native wildlife but also provide important habitat, particularly to birds, when there is no native alternative. In a wetland ecosystem such as a saltmarsh, boxthorn has the potential to increase structural complexity because it can stand as an emergent above surrounding vegetation. We compared bird assemblages and behaviour in saltmarsh vegetation with and without boxthorn in a coastal wetland in south-east Australia. Species assemblage, but not richness, changed with the presence of boxthorn. The presence of singing honeyeaters (Lichenostomus virescens) and white-fronted chats (Epthianura albifrons), the two most common native bird species (based on numerical and spatial dominance), appeared to drive these differences; singing honeyeaters preferred boxthorn while white-fronted chats avoided it. The presence of boxthorn increased the seasonal availability of fruit and flowers, which was reflected by a high frequency of foraging for fruit and nectar where boxthorn was present. In saltmarshes without boxthorn, there was a higher frequency of foraging for insects. Some, but not all, species responded to increased structural complexity and fruit/floral resources provided by boxthorn. Consequently, management by reducing boxthorn is likely to alter bird communities and the usage of sites by some native species, thus management success should consider fine-scale biodiversity objectives, such as managing for particular types or species of birds.

A new semi-automated method for assessing avian acoustic networks reveals that juvenile and adult zebra finches have separate calling networks

Social networks are often inferred from spatial associations, but other parameters like acoustic communication are likely to play a central role in within group interactions. However, it is currently difficult to determine which individual initiates vocalizations, or who responds to whom. To this aim, we designed a method that allows analyzing group vocal network while controlling for spatial networks, by positioning each group member in equidistant individual cages and analyzing continuous vocal interactions semi-automatically. We applied this method to two types of zebra finch groups, composed of either two adult females and two juveniles, or four young adults (juveniles from the first groups). Young often co-occur in the same social group as adults but are likely to have a different social role, which may be reflected in their vocal interactions. Therefore, we tested the hypothesis that the social structure of the group influences the parameters of the group vocal network. We found that groups including juveniles presented periods with higher level of activity than groups composed of young adults. Using two types of analyses (Markov analysis and cross-correlation), we showed that juveniles as well as adults were more likely to respond to individuals of their own age-class (i.e. to call one after another, in terms of turn-taking, and within a short time-window, in terms of time delay). When juveniles turned into adulthood, they showed adult characteristics of vocal patterns. Together our results suggest that vocal behavior changes during ontogeny, and individuals are more strongly connected with individuals of the same age-class within acoustic networks.

Determining the sex of Little Penguins (Eudyptula minor) in northern Bass Strait using morphometric measurements

In avian species with no obvious differences in plumage or body size between the sexes, such as penguins, discriminant function analysis (DFA) of morphometric measurements that display sexual dimorphism can provide a simple and rapid means of determining sex in the field. Like most other penguin species, the Little Penguin (Eudyptula minor) displays sexual dimorphism in bill shape and size. In the present study, discriminant functions (DFs) were developed for sexing adult Little Penguins at two colonies in northern Bass Strait, Victoria, Australia, and their accuracies were compared with those obtained previously in other parts of the species' range. Backwards stepwise DFA indicated that birds at Phillip Island can be sexed with an accuracy of 91% using a single measurement of bill depth (>13.33 mm classed as males). Similar analyses at Gibson Steps produced a DF incorporating bill length, bill depth and head length [although the model with the greatest accuracy when applied to birds from Phillip Island (91%) also contained only bill depth]. Published DFs derived in New Zealand had accuracies of 50–85% when applied to birds from Phillip Island and Gibson Steps, supporting earlier suggestions that DFs are not applicable across subspecies of the Little Penguin. In contrast, there was little difference between the accuracy of the DFs in the present study and that previously derived for the same subspecies in Tasmania when applied to birds from Phillip Island (89%) and Gibson Steps (92%). However, as the degree of variation in bill size within a subspecies is unknown it may still be prudent to derive colony-specific DFs.

Non-uniform bird assemblages in urban environments : the influence of streetscape vegetation

The urban landscape encompasses a broad spectrum of variable environments ranging from remnant patches to highly modified streetscapes. Despite the expansion of urban environments, few studies have examined the influence of urbanization on faunal diversity, particularly in the Southern Hemisphere. In this study, four broad habitat types were recognized in the urban environment, representing a continuum of modification ranging from parks with remnant vegetation to streetscapes dominated by native vegetation and those dominated by exotic vegetation to recently developed streetscapes. Bird censuses were conducted at 36 sites throughout urban Melbourne, with nine sites surveyed in each habitat type. The four habitat types supported significantly different bird communities based on species richness, abundance and composition suggesting that bird assemblages of urban environments are non-uniform. Parks and native streetscapes generally supported fewer introduced species than exotic and recently developed streetscapes. Overall abundance and richness of species were lower in the exotic and recently developed streetscapes than in parks and native streetscapes. Significant differences were also observed in foraging guilds within the four habitat types, with parks having the most foraging guilds and recently developed streetscapes having the fewest. The transition from native to exotic streetscapes saw the progressive loss of insectivorous and nectarivorous species reflecting a reliance by these species on structurally diverse and/or native vegetation for both shelter and food resources. The implementation of effective strategies and incentives which encourage the planting of structurally diverse native vegetation in streetscapes and gardens should be paramount if avian biodiversity is to be retained and enhanced in urban environments. It is also critical to encourage the maintenance of the existing remnant vegetation in the urban environment.

Differential macrohabitat use by birds on an unregulated lowland floodplain of south-eastern Australia

In many lowland floodplains around the world, upriver interferences to flows (weirs, dams, off-takes) have led to much reduced frequency and duration of flooding. As a result, many floodplain wetlands are now inundated relatively rarely if at all. Given regulation of most lowland rivers in southeastern Australia, we assessed use of wetlands by birds in the essentially unregulated Ovens River in northeastern Victoria. Twelve sites (0.4-1.2 ha) were studied after flooding. Four sites were 'permanent billabongs', four were temporary wetlands and the other four were randomly selected woodland sites >60 m from the nearest water body (including the river) acting as 'control' or 'reference' sites. Aquatic birds were not recorded using woodland sites, but many species were differentially associated with either billabongs or temporary wetlands. A surprising number of non-aquatic birds either exclusively or differentially were associated with wetland sites compared with woodland sites. We concluded that heterogeneous macrohabitat will increase local avian biodiversity on lowland floodplains. Moreover, densities and diversity of non-aquatic, woodland species also increased with the presence of wetlands. Temporary wetlands were used differently from permanent billabongs by birds, especially in foraging methods. This suggests that the reinstatement of major flooding on heavily regulated floodplains would be ecologically advantageous for birds by providing foraging and breeding opportunities.

Physiological, morphological and behavioural effects of selecting zebra finches for divergent levels of corticosterone

The effects of environmental stress on the physiology and behaviour of higher vertebrates has become an important avenue of research in recent years. Evidence from recent studies has suggested that the avian stress-related hormone corticosterone (CORT) may play a role in immunocompetence and sexual selection. We tested whether CORT is immunosuppressive by studying humoral and cell-mediated immune responses in populations of captive zebra finches selected for divergent peak levels of CORT. We also investigated whether selection for peak CORT has an effect on the quality of several sexually selected regions of the male zebra finch; in addition we compared morphometric parameters and the dominance ranking in males from the different selection lines. We also tested whether different components of the immune system compete for limited resources. We found that selection for divergent levels of peak CORT had little effect on humoral immunity, male sexual signal quality or dominance ranking. However, contrary to expectations, we did find a positive relationship between CORT titre and cell-mediated immunity, as well as a greater cell-mediated response in the birds selected for high CORT titre than those selected for low CORT titre. Consistent with predictions, significant negative relationships were found between both testosterone and CORT titre on humoral immunity. Birds from the low CORT lines were significantly larger in terms of skeletal size than those from the high CORT lines. Overall, our results suggest that the cell-mediated immune response is associated with a reduction in the humoral response, but only in males, and that there is no simple relationship between peak CORT levels and immune function.

Cholinesterase response in native birds exposed to fenitrothion during locust control operations in Eastern Australia

Huge aggregations of flightless locust nymphs pose a serious threat to agriculture when they reach plague proportions but provide a very visible and nutritious resource for native birds. Locust outbreaks occur in spring and summer months in semiarid regions of Australia. Fenitrothion, an organophosphate pesticide, is sprayed aerially to control locust plagues. To evaluate fenitrothion exposure in birds attending locust outbreaks, we measured total plasma cholinesterase (ChE), butrylcholinesterase (BChE), and acetylcholinesterase (AChE) activities in four avian species captured pre- and postfenitrothion application and ChE reactivation in birds caught postspray only. Eleven of 21 plasma samples from four species had ChE activity below the diagnostic threshold (two standard deviations below the mean ChE activity of prespray samples). Granivorous zebra finches (Taeniopygia guttata) and insectivorous white-winged trillers (Lalage sueurii) had significantly lower mean plasma total ChE, BChE, and AChE activity postspray, while other insectivores, white-browed (Artamus superciliosus) and masked woodswallows (Artamus personatus), did not. Cholinesterase was reactivated in 19 of the 73 plasma samples and in one of three brain samples. We conclude that native bird species are exposed to fenitrothion during locust control operations. This exposure could have detrimental impacts, as both locust outbreaks and avian reproductive events are stimulated by heavy summer rainfall, leading to co-occurrence of locust control and avian breeding activities.

Reduced egg investment can conceal helper effects in cooperatively breeding birds

Cooperative breeding systems are characterized by nonbreeding helpers that assist breeders in offspring care. However, the benefits to offspring of being fed by parents and helpers in cooperatively breeding birds can be difficult to detect. We offer experimental evidence that helper effects can be obscured by an undocumented maternal tactic. In superb fairy-wrens (Malurus cyaneus), mothers breeding in the presence of helpers lay smaller eggs of lower nutritional content that produce lighter chicks, as compared with those laying eggs in the absence of helpers. Helpers compensate fully for such reductions in investment and allow mothers to benefit through increased survival to the next breeding season. We suggest that failure to consider maternal egg-investment strategies can lead to underestimation of the force of selection acting on helping in avian cooperative breeders.

Consequences of maternal yolk testosterone for offspring development and survival : experimental test in a lizard

1. Hormone-mediated maternal effects and developmental plasticity are important sources of phenotypic variation, with potential consequences for trait evolution. Yet our understanding of the importance of maternal hormones for offspring fitness in natural populations is very limited, particularly in non-avian species.

2. We experimentally elevated yolk testosterone by injection of a physiological dose into eggs of the lizard Ctenophorus fordi Storr, to investigate its roles in offspring development, growth and survival.

3. Yolk testosterone did not influence incubation period, basic hatchling morphology or survival under natural conditions. However, there was evidence for increased growth in hatchlings from testosterone-treated eggs, suggesting that maternal hormones have potential fitness consequences in natural populations.

4. The positive effect of prenatal testosterone exposure on postnatal growth could represent a taxonomically widespread developmental mechanism that has evolved into an adaptive maternal effect in some taxa, but remains deleterious or selectively neutral in others.

5. A broader taxonomic perspective should increase our understanding of the role of physiological constraints in the evolution of endocrine maternal effects.

Development of mound-building in Australian brush-turkeys (Alectura lathami) : the role of learning, testosterone and body mass

Australian brush-turkeys (Alectura lathami) hatch in incubation mounds of organic material and have no parental role models to learn from. When raised in outdoor aviaries, without adults, four of six males built incubation mounds at an early age of 4.5–9 months. The two males without mounds were the only ones without detectable levels of testosterone (T) at 4.5 months, whereas body mass did not explain the presence or absence of mound building. At the age of 11 months, all males had detectable T, including those without mounds. This study also investigated the development of social dominance in males kept in mixed-sex groups for 4.5 months. At this latter age, higher-ranked males tended to have higher T levels (P = 0.076), whereas dominance ranks at 4.5 months were not correlated with body mass or size, either at this age or at hatching. Overall, these results suggest that mound building develops without learning, and there is a relationship between T levels and dominance status as well as the absence or presence of mound building. These findings contribute to discussions on the role of learning in behavioural development and the role of T and body mass in avian life history.

An illustration of variable precision rough set theory : The gender classification of the European barn swallow (Hirundo rustica)

This paper introduces a new technique in the investigation of object classification and illustrates the potential use of this technique for the analysis of a range of biological data, using avian morphometric data as an example. The nascent variable precision rough sets (VPRS) model is introduced and compared with the decision tree method ID3 (through a ‘leave n out’ approach), using the same dataset of morphometric measures of European barn swallows (Hirundo rustica) and assessing the accuracy of gender classification based on these measures. The results demonstrate that the VPRS model, allied with the use of a modern method of discretization of data, is comparable with the more traditional non-parametric ID3 decision tree method. We show that, particularly in small samples, the VPRS model can improve classification and to a lesser extent prediction aspects over ID3. Furthermore, through the ‘leave n out’ approach, some indication can be produced of the relative importance of the different morphometric measures used in this problem. In this case we suggest that VPRS has advantages over ID3, as it intelligently uses more of the morphometric data available for the data classification, whilst placing less emphasis on variables with low reliability. In biological terms, the results suggest that the gender of swallows can be determined with reasonable accuracy from morphometric data and highlight the most important variables in this process. We suggest that both analysis techniques are potentially useful for the analysis of a range of different types of biological datasets, and that VPRS in particular has potential for application to a range of biological circumstances.

Heritability of corticosterone response and changes in life history traits during selection in the zebra finch

Vertebrates respond to environmental stressors through the neuro-endocrine stress response, which involves the production of glucocorticoids. We have selected independent, duplicate divergent lines of zebra finches for high, low and control corticosterone responses to a mild stressor. This experiment has shown that over the first four generations, the high lines have demonstrated a significant realized heritability of about 20%. However, the low lines have apparently not changed significantly from controls. This asymmetry in response is potentially because of the fact that all birds appear to be showing increased adaptation to the environment in which they are housed, with significant declines in corticosterone response in control lines as well as low lines. Despite the existence of two- to threefold difference in mean corticosterone titre between high and low lines, there were no observed differences in testosterone titre in adult male birds from the different groups. In addition, there were no consistent, significant differences between the lines in any of the life history variables measured – number of eggs laid per clutch, number of clutches or broods produced per pair, number of fledglings produced per breeding attempt, nor in any of egg, nestling and fledgling mortality. These results highlight the fact that the mechanisms that underlie variation in the avian physiological system can be modified to respond to differences between environments through selection. This adds an additional level of flexibility to the avian physiological system, which will allow it to respond to environmental circumstances.

Spatial ability is impaired and mineralcorticoid receptor mRNA expression in zebra finches (Taeniopygia guttata) selected for acute high corticosterone response to stress

In mammals, stress hormones have profound influences on spatial learning and memory. Here, we investigated whether glucocorticoids influence cognitive abilities in birds by testing a line of zebra finches selectively bred to respond to an acute stressor with high plasma corticosterone (CORT) levels. Cognitive performance was assessed by spatial and visual one-trial associative memory tasks. Task performance in the high CORT birds was compared with that of the random-bred birds from a control breeding line. The birds selected for high CORT in response to an acute stressor performed less well than the controls in the spatial task, but there were no significant differences between the lines in performance during the visual task. The birds from the two lines did not differ in their plasma CORT levels immediately after the performance of the memory tasks; nevertheless, there were significant differences in peak plasma CORT between the lines. The high CORT birds also had significantly lower mineralocorticoid receptor mRNA expression in the hippocampus than the control birds. There was no measurable difference between the lines in glucocorticoid receptor mRNA density in either the hippocampus or the paraventricular nucleus. Together, these findings provide evidence to suggest that stress hormones have important regulatory roles in avian spatial cognition.

Parasites affect song complexity and neural development in a songbird

There is now considerable evidence that female choice drives the evolution of song complexity in many songbird species. However, the underlying basis for such choice remains controversial. The developmental stress hypothesis suggests that early developmental conditions can mediate adult song complexity by perturbing investment in the underlying brain nuclei during their initial growth. Here, we show that adult male canaries (Serinus canaria), infected with malaria (Plasmodium relictum) as juveniles, develop simpler songs as adults compared to uninfected individuals, and exhibit reduced development of the high vocal centre (HVC) song nucleus in the brain. Our results show how developmental stress not only affects the expression of a sexually selected male trait, but also the structure of the underlying song control pathway in the brain, providing a direct link between brain and behaviour. This novel experimental evidence tests both proximate and ultimate reasons for the evolution of complex songs and supports the Hamilton–Zuk hypothesis of parasite-mediated sexual selection. Together, these results propose how developmental costs may help to explain the evolution of honest advertising in the complex songs of birds.