A tangled tale of two teal : population history of the grey Anas gracilis and chestnut teal A. castanea of Australia

Two Australian species of teal (Anseriformes: Anatidae: Anas), the grey teal Anas gracilis and the chestnut teal A. castanea, are remarkable for the zero or near-zero divergence recorded between them in earlier surveys of mitochondrial DNA (mtDNA) diversity. We confirmed this result through wider geographical and population sampling as well as nucleotide sampling in the more rapidly evolving mtDNA control region. Any data set where two species share polymorphism as is the case here can be explained by a model of gene flow through hybridization on one hand or by incomplete lineage sorting on the other hand. Ideally, analysis of such shared polymorphism would simultaneously estimate the likelihood of both phenomena. To do this, we used the underlying principle of the IMa package to explore ramifications to understanding population histories of A. gracilis and A. castanea. We cannot reject that hybridization occurs between the two species but an equally or more plausible finding for their nearly zero divergence is incomplete sorting following very recent divergence between the two, probably in the mid-late Pleistocene. Our data add to studies that explore intermediate stages in the evolution of reciprocal monophyly and paraphyletic or polyphyletic relationships in mtDNA diversity among widespread Australian birds.

What drives long-distance movements in the nomadic Grey Teal Anas gracilis in Australia?

In contrast to northern temperate environments, where day length and temperature changes are obvious proximate cues for movement to resource-rich breeding habitats, the cues for movement used by birds in an often resource-poor, stochastic environment are less obvious. We recorded long-distance movements of 23 Grey Teal Anas gracilis using satellite telemetry for up to 879 days and examined the relationship between those movements and environmental factors, such as heavy rainfall and flooding, at the destination site. We identified 32 long-distance [> 150 km) movements that met our criterion for minimally interrupted flight between origin and destination. Thirteen of these flights coincided with rainfall and/or flooding events up to 1050 km from the origin. However, some ducks moved without any clear beneficial conditions at the destination onto small wetlands in regions with little surface water. The data suggest that there are two types of long-distance movement - ranging and directed. These flights occurred over distances up to 1200 km across the arid inland. The rates and distances of movement suggest that long-distance movements of Grey Teal entail high energy costs as in waterfowl elsewhere. We conclude that the proximate controls of directIn contrast to northern temperate environments, where day length and temperature changes are obvious proximate cues for movement to resource-rich breeding habitats, the cues for movement used by birds in an often resource-poor, stochastic environment are less obvious. We recorded long-distance movements of 23 Grey Teal Anas gracilis using satellite telemetry for up to 879 days and examined the relationship between those movements and environmental factors, such as heavy rainfall and flooding, at the destination site. We identified 32 long-distance (> 150 km) movements that met our criterion for minimally interrupted flight between origin and destination. Thirteen of these flights coincided with rainfall and/or flooding events up to 1050 km from the origin. However, some ducks moved without any clear beneficial conditions at the destination onto small wetlands in regions with little surface water. The data suggest that there are two types of long-distance movement – ranging and directed. These flights occurred over distances up to 1200 km across the arid inland. The rates and distances of movement suggest that long-distance movements of Grey Teal entail high energy costs as in waterfowl elsewhere. We conclude that the proximate controls of directed movements need not be very different from those of their temperate counterparts.ed movements need not be very different from those of their temperate counterparts.

Movements of a nomadic waterfowl, Grey Teal Anas gracilis, across inland Australia – results from satellite telemetry spanning fifteen months

We used lightweight satellite transmitters to follow the movements of 17 Grey Teal Anas gracilis between September 2003 and November 2004 in two contrasting landscapes, the agricultural districts of southern Australia and the desert landscapes of the interior. Tagged birds moved large distances (up to 343 km) between occupied sites in a short period (hours), remained in the vicinity of those sites for extended periods (months), ventured up to 453 km from their point of release and travelled more than 2000 km in one year. We describe patterns of movement in a nomadic waterfowl for 15 months from September 2003, a period of severe drought. Based on the current analysis there appears to be no remarkable difference in the observed patterns of movement of those released in the agricultural landscapes and those released in the desert. As in waterfowl elsewhere, movements appear to occur in response to changes in local food abundance that threaten survival or the imperative to move in order to breed successfully. In Grey Teal, the proximate cues for movement transcend the local landscape and some birds are responding to temporary cues hundreds of kilometres distant. This is in contrast to the universal seasonal cues associated with migration systems elsewhere.

Multilocus phylogeography of Australian teals (Anas spp.) : a case study of the relationship between vagility and genetic structure

Biogeographic barriers potentially restrict gene flow but variation in dispersal or vagility can influence the effectiveness of these barriers among different species and produce characteristic patterns of population genetic structure. The objective of this study was to investigate interspecific and intraspecific genetic structure in two closely related species that differ in several life-history characteristics. The grey teal Anas gracilis is geographically widespread throughout Australia with a distribution that crosses several recognized biogeographic barriers. This species has high vagility as its extensive movements track broad-scale patterns in rainfall. In contrast, the closely related chestnut teal A. castanea is endemic to the mesic southeastern and southwestern regions of Australia and is more sedentary. We hypothesized that these differences in life-history characteristics would result in more pronounced population structuring in the chestnut teal. We sequenced five nuclear loci (nuDNA) for 49 grey teal and 23 chestnut teal and compared results to published mitochondrial DNA (mtDNA) sequences. We used analysis of molecular variance to examine population structure, and applied coalescent based approaches to estimate demographic parameters. As predicted, chestnut teal were more strongly structured at both mtDNA and nuDNA (ΦST= 0.163 and 0.054, respectively) than were grey teal (ΦST < 0.0001 for both sets of loci). Surprisingly, a greater proportion of the total genetic variation was partitioned among populations within species (ΦSC= 0.014 and 0.047 for nuDNA and mtDNA, respectively) than between the two species (ΦCT < 0.0001 for both loci). The ‘Isolation with Migration’ coalescent model suggested a late Pleistocene divergence between the taxa, but remarkably, a deeper divergence between the southeastern and southwestern populations of chestnut teal. We conclude that dispersal potential played a prominent role in the structuring of populations within these species and that divergent selection associated with ecology and life history traits likely contributed to rapid and recent speciation in this pair.

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.

Fuelling rates of garganey (Anas querquedula) staging in the Camargue, Southern France, during spring migration

Most species of long-distance migratory birds put on energy stores to fuel their travels. However, recent studies have highlighted the potential costs associated with carrying too much fuel, either through increased predation risk or decreased flight efficiency. Consequently, it is now widely accepted that migratory birds should carry optimal rather than maximum fuel loads. Information from 372 garganey (Anas querquedula) ringed and recaptured at least once during the same spring in the Camargue, southern France, was used to document fuelling rates of individual ducks in relation to environmental variation and individual variation in condition. On average, garganey added very little fuel stores in the Camargue (mean gain per day = 0.33 g, less than 0.5% of mean body-mass in total over an average stay of 5 days). Fuelling rates were negatively correlated with body mass at capture, but it cannot be excluded that this pattern was a statistical artefact. Given their body-mass at ringing, garganey could potentially still fly long distances when they stop in the Camargue. It is therefore likely that the aim of their stay in southern France is more for resting than refuelling, a finding that may have implications for the proper management of stop-over sites.

Wingbeat frequency and the body drag anomaly: wind-tunnel observations on a thrush nightingale (Luscinia Luscinia) and a teal (Anas crecca)

A teal (Anas crecca) and a thrush nightingale (Luscinia luscinia) were trained to fly in the Lund wind tunnel for periods of up to 3 and 16 h respectively. Both birds flew in steady flapping flight, with such regularity that their wingbeat frequencies could be determined by viewing them through a shutter stroboscope. When flying at a constant air speed, the teal's wingbeat frequency varied with the 0.364 power of the body mass and the thrush nightingale's varied with the 0.430 power. Both exponents differed from zero, but neither differed from the predicted value (0.5) at the 1 % level of significance. The teal continued to flap steadily as the tunnel tilt angle was varied from -1° (climb) to +6° (descent), while the wingbeat frequency declined progressively by about 11%. In both birds, the plot of wingbeat frequency against air speed in level flight was U-shaped, with small but statistically significant curvature. We identified the minima of these curves with the minimum power speed (Vmp) and found that the values predicted for Vmp, using previously published default values for the required variables, were only about two-thirds of the observed minimum-frequency speeds. The discrepancy could be resolved if the body drag coefficients (CDb) of both birds were near 0.08, rather than near 0.40 as previously assumed. The previously published high values for body drag coefficients were derived from wind-tunnel measurements on frozen bird bodies, from which the wings had been removed, and had long been regarded as anomalous, as values below 0.01 are given in the engineering literature for streamlined bodies. We suggest that birds of any size that have well-streamlined bodies can achieve minimum body drag coefficients of around 0.05 if the feet can be fully retracted under the flank feathers. In such birds, field observations of flight speeds may need to be reinterpreted in the light of higher estimates of Vmp. Estimates of the effective lift:drag ratio and range can also be revised upwards. Birds that have large feet or trailing legs may have higher body drag coefficients. The original estimates of around CDb=0.4 could be correct for species, such as pelicans and large herons, that also have prominent heads. We see no evidence for any progressive reduction of body drag coefficient in the Reynolds number range covered by our experiments, that is 21600-215 000 on the basis of body cross-sectional diameter.

Proximate cues to phases of movement in a highly dispersive waterfowl, anas superciliosa

BACKGROUND: Waterfowl can exploit distant ephemeral wetlands in arid environments and provide valuable insights into the response of birds to rapid environmental change, and behavioural flexibility of avian movements. Currently much of our understanding of behavioural flexibility of avian movement comes from studies of migration in seasonally predictable biomes in the northern hemisphere. We used GPS transmitters to track 20 Pacific black duck (Anas superciliosa) in arid central Australia. We exploited La Niña conditions that brought extensive flooding, so allowing a rare opportunity to investigate how weather and other environmental factors predict initiation of long distance movement toward freshly flooded habitats. We employed behavioural change point analysis to identify three phases of movement: sedentary, exploratory and long distance oriented movement. We then used random forest models to determine the ability of meteorological and remote sensed landscape variables to predict initiation of these phases. RESULTS: We found that initiation of exploratory movement phases is influenced by fluctuations in local weather conditions and accumulated rainfall in the landscape. Initiation of long distance movement phases was found to be highly individualistic with minor influence from local weather conditions. CONCLUSIONS: Our study reveals how individuals utilise local conditions to respond to changes in resource distribution at broad scales. Our findings suggest that individual movement decisions of dispersive birds are informed by the integration of multiple weather cues operating at different temporal and spatial scales.

Weak negative associations between avian influenza virus infection and movement behaviour in a key host species, the mallard Anas platyrhynchos

Animal movements may contribute to the spread of pathogens. In the case of avian influenza virus, [migratory] birds have been suggested to play a role in the spread of some highly pathogenic strains (e.g. H5N1, H5N8), as well as their low pathogenic precursors which circulate naturally in wild birds. For a better understanding of the emergence and spread of both highly pathogenic (HPAIV) and low pathogenic avian influenza virus (LPAIV), the potential effects of LPAIVs on bird movement need to be evaluated. In a key host species, the mallard Anas platyrhynchos, we tested whether LPAIV infection status affected daily local (< 100 m) and regional (> 100 m) movements by comparing movement behaviour 1) within individuals (captured and sampled at two time points) and 2) between individuals (captured and sampled at one time point). We fitted free-living adult males with GPS loggers throughout the autumn LPAIV infection peak, and sampled them for LPAIV infection at logger deployment and at logger removal on recapture. Within individuals, we found no association between LPAIV infection and daily local and regional movements. Among individuals, daily regional movements of LPAIV infected mallards in the last days of tracking were lower than those of non-infected birds. Moreover, these regional movements of LPAIV infected birds were additionally reduced by poor weather conditions (i.e. increased wind and/or precipitation and lower temperatures). Local movements of LPAIV infected birds in the first days of tracking were higher when temperature decreased. Our study thus demonstrates that bird-assisted dispersal rate of LPAIV may be lower on a regional scale than expected on the basis of the movement behaviour of non-infected birds. Our study underlines the importance of understanding the impact of pathogen infection on host movement in order to assess its potential role in the emergence and spread of infectious diseases.

Animal movement in dynamic landscapes : interaction between behavioural strategies and resource distributions

Most ecological and evolutionary processes are thought to critically depend on dispersal and individual movement but there is little empirical information on the movement strategies used by animals to find resources. In particular, it is unclear whether behavioural variation exists at all scales, or whether behavioural decisions are primarily made at small spatial scales and thus broad-scale patterns of movement simply reflect underlying resource distributions. We evaluated animal movement responses to variable resource distributions using the grey teal (Anas gracilis) in agricultural and desert landscapes in Australia as a model system. Birds in the two landscapes differed in the fractal dimension of their movement paths, with teal in the desert landscape moving less tortuously overall than their counterparts in the agricultural landscape. However, the most striking result was the high levels of individual variability in movement strategies, with different animals exhibiting different responses to the same resources. Teal in the agricultural basin moved with both high and low tortuosity, while teal in the desert basin primarily moved using low levels of tortuosity. These results call into question the idea that broad-scale movement patterns simply reflect underlying resource distributions, and suggest that movement responses in some animals may be behaviourally complex regardless of the spatial scale over which movement occurs.

Use of satellite telemetry on small-bodied waterfowl in Australia

The nomadic or dispersive movements of many Australian waterfowl in response to irregular environmental cues make satellite telemetry studies the only means by which these long-distance movements can be tracked in real time. Unlike some large-bodied soaring species, attaching satellite transmitters to small-bodied waterfowl (<1 kg) is not straightforward because ducks have high wing loadings and need to maintain active flapping to stay aloft. In the present paper, we detail one harness design and attachment method that enabled us to track grey teal (Anas gracilis) for up to 879 days. In addition, we detail rates of data loss, changes in data quality over time and variation in data quality from solar-powered satellite-tags deployed on ducks in Australia and Papua New Guinea. Up to 68% of all locational fixes have a nominal accuracy of less than 1 km, and satellite-tags deployed on wild birds can provide up to 22 location fixes per day and store enough energy during the day to run continuously throughout the night.

Small seed size increases the potential for dispersal of wetland plants by ducks

1. Long-distance dispersal (LDD) is important in plants of dynamic and ephemeral habitats. For plants of dynamic wetland habitats, waterfowl are generally considered to be important LDD vectors. However, in comparison to the internal (endozoochorous) dispersal of terrestrial plants by birds, endozoochorous dispersal of wetland plants by waterfowl has received little attention. We quantified the capacity for endozoochorous dispersal of wetland plants by waterfowl and identified the mechanisms underlying successful dispersal, by comparing the dispersal capacities of a large number of wetland plant species.

2. We selected 23 common plant species from dynamic wetland habitats and measured their seed characteristics. We fed seeds of all species to mallards (Anas platyrhynchos), a common and highly omnivorous duck species, and quantified seed gut survival, gut passage speed and subsequent germination. We then used a simple model to calculate seed dispersal distances.

3. In total 21 of the 23 species can be dispersed by mallards, with intact seed retrieval and subsequent successful germination of up to 32% of the ingested seeds. The species that pass fastest through the digestive tract of the mallards are retrieved in the greatest numbers (up to 54%) and germinate best (up to 87%). These are the species with the smallest seeds. Seed coat thickness plays only a minor role in determining intact passage through the mallard gut, but determines if ingestion enhances or reduces germination in comparison to control seeds.

4. Model calculations estimate that whereas the largest seeds can hardly be dispersed by mallards, most seeds can be dispersed up to 780 km, and the smallest seeds up to 3000 km, by mallards during migration.

5. Synthesis. This study demonstrates the mechanism underlying successful endozoochorous dispersal of wetland plant seeds by mallards: small seed size promotes rapid, and hence intact and viable, passage through the mallard gut. Mallards can disperse wetland plant seeds of all but the largest-seeded species successfully in relatively large numbers (up to 32% of ingested seeds) over long distances (up to thousands of kilometres) and are therefore important dispersal vectors.

Quantification of allochthonous nutrient input into freshwater bodies by herbivorous waterbirds

1. Waterbirds are considered to import large quantities of nutrients to freshwater bodies but quantification of these loadings remains problematic. We developed two general models to calculate such allochthonous nutrient inputs considering food intake, foraging behaviour and digestive performance of waterbirds feeding in terrestrial habitats: an intake model (IM), mainly based on an allometric relationship for energy requirements and a dropping model (DM), based on allometric relationships for defaecation.

2. Reviewed data of nitrogen (N) and phosphorus (P) content of herbivorous food varied according to diet type (foliage, seeds and roots), season and fertilization. For model parameterization average foliage diet contained 38.20 mg N g⁻¹ and 3.21 mg P g⁻¹ (dry weight), whereas mean faeces composition was 45.02 mg N g⁻¹ and 6.18 mg P g⁻¹.

3. Daily allochthonous nutrient input increased with body mass ranging from 0.29 g N and 0.03 g P in teals Anas crecca to 5.69 g N and 0.57 g P in mute swans Cygnus olor. Results from IM differed from those of DM from ducks to swans by 63–108% for N and by −4 to 23% for P. Model uncertainty was lowest for the IM and mainly caused by variation in estimates of food retention time (RT). In DM food RT and dropping mass determined model uncertainty in similar extent.

4. Exemplarily applying the models to Dutch wetlands resulted in mean annual contribution of herbivorous waterbirds to allochthonous nutrient loading of 382.8 ± 167.1 tonnes N a⁻¹and 34.7 ± 2.3 tonnes P a⁻¹, respectively, which corresponds to annual surface-water loadings of 1.07 kg N ha⁻¹ and 0.10 kg P ha⁻¹.

5. There was a distinct seasonal pattern with peak loadings in January, when bird abundances were highest. Lowest inputs were in August, when bird abundance and nutrient content in food was low and birds foraged less in terrestrial habitats. Three-quarters of all nutrient input was contributed by greater white-fronted goose Anser albifrons, greylag goose Anser anser, wigeon Anas penelope and barnacle goose Branta leucopsis alone.

6. We provide general, easy to use calculation methods for the estimation of allochthonous nutrient inputs by waterbirds, which are applicable to a range of waterbird species, a variety of potential diets and feeding behaviours, and across spatial scales. Such tools may greatly assist in the planning and execution of management actions for wetland nutrient budgets.

Effects of infection-induced migration delays on the epidemiology of avian influenza in wild mallard populations

Wild waterfowl populations form a natural reservoir of Avian Influenza (AI) virus, and fears exist that these birds may contribute to an AI pandemic by spreading the virus along their migratory flyways. Observational studies suggest that individuals infected with AI virus may delay departure from migratory staging sites. Here, we explore the epidemiological dynamics of avian influenza virus in a migrating mallard (Anas platyrhynchos) population with a specific view to understanding the role of infection-induced migration delays on the spread of virus strains of differing transmissibility. We develop a host-pathogen model that combines the transmission dynamics of influenza with the migration, reproduction and mortality of the host bird species. Our modeling predicts that delayed migration of individuals influences both the timing and size of outbreaks of AI virus. We find that (1) delayed migration leads to a lower total number of cases of infection each year than in the absence of migration delay, (2) when the transmission rate of a strain is high, the outbreak starts at the staging sites at which birds arrive in the early part of the fall migration, (3) when the transmission rate is low, infection predominantly occurs later in the season, which is further delayed when there is a migration delay. As such, the rise of more virulent AI strains in waterfowl could lead to a higher prevalence of infection later in the year, which could change the exposure risk for farmed poultry. A sensitivity analysis shows the importance of generation time and loss of immunity for the effect of migration delays. Thus, we demonstrate, in contrast to many current transmission risk models solely using empirical information on bird movements to assess the potential for transmission, that a consideration of infection-induced delays is critical to understanding the dynamics of AI infection along the entire flyway.

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.