A predictive model of avian natal dispersal distance provides prior information for investigating response to landscape change

1. Informative Bayesian priors can improve the precision of estimates in ecological studies or estimate parameters for which little or no information is available. While Bayesian analyses are becoming more popular in ecology, the use of strongly informative priors remains rare, perhaps because examples of informative priors are not readily available in the published literature.

2. Dispersal distance is an important ecological parameter, but is difficult to measure and estimates are scarce. General models that provide informative prior estimates of dispersal distances will therefore be valuable.

3. Using a world-wide data set on birds, we develop a predictive model of median natal dispersal distance that includes body mass, wingspan, sex and feeding guild. This model predicts median dispersal distance well when using the fitted data and an independent test data set, explaining up to 53% of the variation.

4. Using this model, we predict a priori estimates of median dispersal distance for 57 woodland-dependent bird species in northern Victoria, Australia. These estimates are then used to investigate the relationship between dispersal ability and vulnerability to landscape-scale changes in habitat cover and fragmentation.

5. We find evidence that woodland bird species with poor predicted dispersal ability are more vulnerable to habitat fragmentation than those species with longer predicted dispersal distances, thus improving the understanding of this important phenomenon.

6. The value of constructing informative priors from existing information is also demonstrated. When used as informative priors for four example species, predicted dispersal distances reduced the 95% credible intervals of posterior estimates of dispersal distance by 8-19%. Further, should we have wished to collect information on avian dispersal distances and relate it to species' responses to habitat loss and fragmentation, data from 221 individuals across 57 species would have been required to obtain estimates with the same precision as those provided by the general model.

Role of position 627 of PB2 and the multibasic cleavage site of the hemagglutinin in the virulence of H5N1 avian influenza virus in chickens and ducks

Highly pathogenic H5N1 avian influenza viruses have caused major disease outbreaks in domestic and free-living birds with transmission to humans resulting in 59% mortality amongst 564 cases. The mutation of the amino acid at position 627 of the viral polymerase basic-2 protein (PB2) from glutamic acid (E) in avian isolates to lysine (K) in human isolates is frequently found, but it is not known if this change affects the fitness and pathogenicity of the virus in birds. We show here that horizontal transmission of A/Vietnam/1203/2004 H5N1 (VN/1203) virus in chickens and ducks was not affected by the change of K to E at PB2-627. All chickens died between 21 to 48 hours post infection (pi), while 70% of the ducks survived infection. Virus replication was detected in chickens within 12 hours pi and reached peak titers in spleen, lung and brain between 18 to 24 hours for both viruses. Viral antigen in chickens was predominantly in the endothelium, while in ducks it was present in multiple cell types, including neurons, myocardium, skeletal muscle and connective tissues. Virus replicated to a high titer in chicken thrombocytes and caused upregulation of TLR3 and several cell adhesion molecules, which may explain the rapid virus dissemination and location of viral antigen in endothelium. Virus replication in ducks reached peak values between 2 and 4 days pi in spleen, lung and brain tissues and in contrast to infection in chickens, thrombocytes were not involved. In addition, infection of chickens with low pathogenic VN/1203 caused neuropathology, with E at position PB2-627 causing significantly higher infection rates than K, indicating that it enhances virulence in chickens.

From food to offspring down : tissue-specific discrimination and turn-over of stable isotopes in herbivorous waterbirds and other avian foraging guilds

Isotopic discrimination and turn-over are fundamental to the application of stable isotope ecology in animals. However, detailed information for specific tissues and species are widely lacking, notably for herbivorous species. We provide details on tissue-specific carbon and nitrogen discrimination and turn-over times from food to blood, feathers, claws, egg tissues and offspring down feathers in four species of herbivorous waterbirds. Source-to-tissue discrimination factors for carbon (δ¹³C) and nitrogen stable isotope ratios (δ¹⁵N) showed little variation across species but varied between tissues. Apparent discrimination factors ranged between −0.5 to 2.5‰ for δ¹³C and 2.8 to 5.2‰ for δ¹⁵N, and were more similar between blood components than between keratinous tissues or egg tissue. Comparing these results with published data from other species we found no effect of foraging guild on discrimination factors for carbon but a significant foraging-guild effect for nitrogen discrimination factors.

Turn-over of δ¹³C in tissues was most rapid in blood plasma, with a half-life of 4.3 d, whereas δ¹³C in blood cells had a half-life of approximately 32 d. Turn-over times for albumen and yolk in laying females were similar to those of blood plasma, at 3.2 and 6.0 d respectively. Within yolk, we found decreasing half-life times of δ¹³C from inner yolk (13.3 d) to outer yolk (3.1 d), related to the temporal pattern of tissue formation.

We found similarities in tissue-specific turn-over times across all avian species studied to date. Yet, while generalities regarding discrimination factors and tissue turn-over times can be made, a large amount of variation remains unexplained.

Variation in postsampling treatment of avian blood affects ecophysiological interpretations

The fluid component of blood is widely used in ecophysiological investigations, including measures of immune function and stable isotope ecology. After blood collection, delayed separation of blood extracellular fluids from red blood cells is known to affect the concentration of a wide range of biochemical compounds in the resulting fluid, as does prevention of clotting (producing plasma) when compared with blood allowed to clot (producing serum). One challenge when investigating immune function and stable isotope ecology, therefore, is discriminating variation because of the effect of the biological factors of interest from potential methodological artefacts. This study assesses how seven widely used measures of immune function and stable isotope composition respond both to delayed separation of the cellular and fluid components and to the clotting of blood samples from two species of waterfowl. Samples that remained uncentrifuged for up to 12 h did not differ from those centrifuged within 15 min of sampling from the same individuals, indicating that samples from a wide range of field conditions may remain highly comparable. However, the outcome of three of the four immunological assays and two of the three isotopic analyses was highly dependent on the type of fluid, with higher immunological activity and higher relative concentrations of heavy carbon and total nitrogen in plasma compared to serum. Researchers interested in immune function and stable isotope ecology may obtain the most useful results by ensuring that they use a single fluid type in their investigations.

Avian influenza from an ecohealth perspective

To understand and better control AI outbreaks, not only is it necessary to understand the biology of influenza viruses but also the natural history of the hosts in which these viruses multiply and the different environments in which the hosts and viruses interact. This includes the anthropogenic factors that have influenced where, whether and how avian influenza (AI) viruses can replicate and transmit between wild birds and poultry, and between poultry and mammals, including factors influencing uptake and application of appropriate control and preventive measures for AI. This disease represents one of the best examples of the need for a ‘One Health’ approach to understand and tackle disease with an increasing need to comprehend and unravel the environmental and ecology drivers that affect the virus host interactions. This forum piece seeks to bring together these aspects through a review of recent outbreaks and how a deeper understanding of all three aspects, the virus, the host and the environment, can help us better manage future outbreaks.

Predicting avian distributions to evaluate spatiotemporal overlap with locust control operations in eastern Australia.

Locusts and grasshoppers cause considerable economic damage to agriculture worldwide. The Australian Plague Locust Commission uses multiple pesticides to control locusts in eastern Australia. Avian exposure to agricultural pesticides is of conservation concern, especially in the case of rare and threatened species. The aim of this study was to evaluate the probability of pesticide exposure of native avian species during operational locust control based on knowledge of species occurrence in areas and times of application. Using presence-absence data provided by the Birds Australia Atlas for 1998 to 2002, we developed a series of generalized linear models to predict avian occurrences on a monthly basis in 0.5 degrees grid cells for 280 species over 2 million km2 in eastern Australia. We constructed species-specific models relating occupancy patterns to survey date and location, rainfall, and derived habitat preference. Model complexity depended on the number of observations available. Model output was the probability of occurrence for each species at times and locations of past locust control operations within the 5-year study period. Given the high spatiotemporal variability of locust control events, the variability in predicted bird species presence was high, with 108 of the total 280 species being included at least once in the top 20 predicted species for individual space-time events. The models were evaluated using field surveys collected between 2000 and 2005, at sites with and without locust outbreaks. Model strength varied among species. Some species were under- or over-predicted as times and locations of interest typically did not correspond to those in the prediction data set and certain species were likely attracted to locusts as a food source. Field surveys demonstrated the utility of the spatially explicit species lists derived from the models but also identified the presence of a number of previously unanticipated species. These results also emphasize the need for special consideration of rare and threatened species that are poorly predicted by presence-absence models. This modeling exercise was a useful a priori approach in species risk assessments to identify species present at times and locations of locust control applications, and to discover gaps in our knowledge and need for further focused data collection.

Odour-based discrimination of subspecies, species and sexes in an avian species complex, the crimson rosella

Olfaction is an ancient sensory capability, and yet while it is now widely recognized that birds have olfactory mechanisms, use of the sense within a social context has been largely overlooked. In our study, we aimed to determine, for the first time, whether plumage odour may contribute to avian subspecies discrimination. We used a species complex, the crimson rosella, Platycercus elegans, which exhibits large geographical and phenotypic differences. Across 2 years in a wild population of P.elegans elegans we tested whether females at the nest could: (1) discriminate odours of conspecifics; (2) discriminate odours of subspecies; (3) discriminate odours of sexes of conspecifics; and (4) habituate at different rates to odour treatments. We found that female response differed between odours of feathers of consubspecifics, heterosubspecifics, heterospecific controls and sham controls and between odours of sexes of conspecifics. Across all odour treatments, we found habituation to the odour and the rate of habituation differed between odour treatments. Our results indicate that P.e. elegans females are able to discriminate conspecifics, consubspecifics and sexes based on plumage odour. To our knowledge, this is the first work to show that birds of a certain subspecies can discriminate the odour of its own subspecies from that of other subspecies. Our findings suggest that olfaction in birds may play a larger role than hitherto considered, and may even act as a signal to maintain or promote population divergence. © 2014 The Association for the Study of Animal Behaviour.

Effects of Mitochondrial DNA Rate Variation on Reconstruction of Pleistocene Demographic History in a Social Avian Species, Pomatostomus superciliosus

Mitochondrial sequence data is often used to reconstruct the demographic history of Pleistocene populations in an effort to understand how species have responded to past climate change events. However, departures from neutral equilibrium conditions can confound evolutionary inference in species with structured populations or those that have experienced periods of population expansion or decline. Selection can affect patterns of mitochondrial DNA variation and variable mutation rates among mitochondrial genes can compromise inferences drawn from single markers. We investigated the contribution of these factors to patterns of mitochondrial variation and estimates of time to most recent common ancestor (TMRCA) for two clades in a co-operatively breeding avian species, the white-browed babbler Pomatostomus superciliosus. Both the protein-coding ND3 gene and hypervariable domain I control region sequences showed departures from neutral expectations within the superciliosus clade, and a two-fold difference in TMRCA estimates. Bayesian phylogenetic analysis provided evidence of departure from a strict clock model of molecular evolution in domain I, leading to an over-estimation of TMRCA for the superciliosus clade at this marker. Our results suggest mitochondrial studies that attempt to reconstruct Pleistocene demographic histories should rigorously evaluate data for departures from neutral equilibrium expectations, including variation in evolutionary rates across multiple markers. Failure to do so can lead to serious errors in the estimation of evolutionary parameters and subsequent demographic inferences concerning the role of climate as a driver of evolutionary change. These effects may be especially pronounced in species with complex social structures occupying heterogeneous environments. We propose that environmentally driven differences in social structure may explain observed differences in evolutionary rate of domain I sequences, resulting from longer than expected retention times for matriarchal lineages in the superciliosus clade.

Migratory birds reinforce local circulation of avian influenza viruses

Migratory and resident hosts have been hypothesized to fulfil distinct roles in infectious disease dynamics. However, the contribution of resident and migratory hosts to wildlife infectious disease epidemiology, including that of low pathogenic avian influenza virus (LPAIV) in wild birds, has largely remained unstudied. During an autumn H3 LPAIV epizootic in free-living mallards (Anas platyrhynchos) - a partially migratory species - we identified resident and migratory host populations using stable hydrogen isotope analysis of flight feathers. We investigated the role of migratory and resident hosts separately in the introduction and maintenance of H3 LPAIV during the epizootic. To test this we analysed (i) H3 virus kinship, (ii) temporal patterns in H3 virus prevalence and shedding and (iii) H3-specific antibody prevalence in relation to host migratory strategy. We demonstrate that the H3 LPAIV strain causing the epizootic most likely originated from a single introduction, followed by local clonal expansion. The H3 LPAIV strain was genetically unrelated to H3 LPAIV detected both before and after the epizootic at the study site. During the LPAIV epizootic, migratory mallards were more often infected with H3 LPAIV than residents. Low titres of H3-specific antibodies were detected in only a few residents and migrants. Our results suggest that in this LPAIV epizootic, a single H3 virus was present in resident mallards prior to arrival of migratory mallards followed by a period of virus amplification, importantly associated with the influx of migratory mallards. Thus migrants are suggested to act as local amplifiers rather than the often suggested role as vectors importing novel strains from afar. Our study exemplifies that a multifaceted interdisciplinary approach offers promising opportunities to elucidate the role of migratory and resident hosts in infectious disease dynamics in wildlife.

Transfer of maternal antibodies against avian influenza virus in mallards (Anas platyrhynchos)

Maternal antibodies protect chicks from infection with pathogens early in life and may impact pathogen dynamics due to the alteration of the proportion of susceptible individuals in a population. We investigated the transfer of maternal antibodies against avian influenza virus (AIV) in a key AIV host species, the mallard (Anas platyrhynchos). Combining observations in both the field and in mallards kept in captivity, we connected maternal AIV antibody concentrations in eggs to (i) female body condition, (ii) female AIV antibody concentration, (iii) egg laying order, (iv) egg size and (v) embryo sex. We applied maternity analysis to the eggs collected in the field to account for intraspecific nest parasitism, which is reportedly high in Anseriformes, detecting parasitic eggs in one out of eight clutches. AIV antibody prevalence in free-living and captive females was respectively 48% and 56%, with 43% and 24% of the eggs receiving these antibodies maternally. In both field and captive study, maternal AIV antibody concentrations in egg yolk correlated positively with circulating AIV antibody concentrations in females. In the captive study, yolk AIV antibody concentrations correlated positively with egg laying order. Female body mass and egg size from the field and captive study, and embryos sex from the field study were not associated with maternal AIV antibody concentrations in eggs. Our study indicates that maternal AIV antibody transfer may potentially play an important role in shaping AIV infection dynamics in mallards.

Minor differences in body condition and immune status between avian influenza virus-infected and noninfected mallards: a sign of coevolution?

Wildlife pathogens can alter host fitness. Low pathogenic avian influenza virus (LPAIV) infection is thought to have negligible impacts on wild birds; however, effects of infection in free-living birds are largely unstudied. We investigated the extent to which LPAIV infection and shedding were associated with body condition and immune status in free-living mallards (Anas platyrhynchos), a partially migratory key LPAIV host species. We sampled mallards throughout the species' annual autumn LPAIV infection peak, and we classified individuals according to age, sex, and migratory strategy (based on stable hydrogen isotope analysis) when analyzing data on body mass and five indices of immune status. Body mass was similar for LPAIV-infected and noninfected birds. The degree of virus shedding from the cloaca and oropharynx was not associated with body mass. LPAIV infection and shedding were not associated with natural antibody (NAbs) and complement titers (first lines of defense against infections), concentrations of the acute phase protein haptoglobin (Hp), ratios of heterophils to lymphocytes (H:L ratio), and avian influenza virus (AIV)-specific antibody concentrations. NAbs titers were higher in LPAIV-infected males and local (i.e., short distance) migrants than in infected females and distant (i.e., long distance) migrants. Hp concentrations were higher in LPAIV-infected juveniles and females compared to infected adults and males. NAbs, complement, and Hp levels were lower in LPAIV-infected mallards in early autumn. Our study demonstrates weak associations between infection with and shedding of LPAIV and the body condition and immune status of free-living mallards. These results may support the role of mallards as asymptomatic carriers of LPAIV and raise questions about possible coevolution between virus and host.