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  • 1.
    Avril, Alexis
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Grosbois, Vladimir
    CIRAD, France.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Georgia, USA.
    Gaidet, Nicolas
    CIRAD, France.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Olsen, Björn
    Uppsala University.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Capturing individual-level parameters of influenza A virus dynamics in wild ducks using multistate models2016In: Journal of Applied Ecology, ISSN 0021-8901, E-ISSN 1365-2664, Vol. 53, no 4, p. 1289-1297Article in journal (Refereed)
    Abstract [en]

    Disease prevalence in wildlife is governed by epidemiological parameters (infection and recovery rates) and response to infection, both of which vary within and among individual hosts. Studies quantifying these individual-scale parameters and documenting their source of variation in wild hosts are fundamental for predicting disease dynamics. Such studies do not exist for the influenza A virus (IAV), despite its strong impact on the global economy and public health. Using capture-recaptures of 3500 individual mallards Anas platyrhynchos during seven migration seasons at a stopover site in southern Sweden, we provide the first empirical description of the individual-based mechanisms of IAV dynamics in a wild reservoir host. For most years, prevalence and risk of IAV infection peaked at a single time during the autumn migration season, but the timing, shape and intensity of the infection curve showed strong annual heterogeneity. In contrast, the seasonal pattern of recovery rate only varied in intensity across years. Adults and juveniles displayed similar seasonal patterns of infection and recovery each year. However, compared to adults, juveniles experienced twice the risk of becoming infected, whereas recovery rates were similar across age categories. Finally, we did not find evidence that infection influenced the timing of emigration.Synthesis and applications. Our study provides robust empirical estimates of epidemiological parameters for predicting influenza A virus (IAV) dynamics. However, the strong annual variation in infection curves makes forecasting difficult. Prevalence data can provide reliable surveillance indicators as long as they catch the variation in infection risk. However, individual-based monitoring of infection is required to verify this assumption in areas where surveillance occurs. In this context, monitoring of captive sentinel birds kept in close contact with wild birds is useful. The fact that infection does not impact the timing of migration underpins the potential for mallards to spread viruses rapidly over large geographical scales. Hence, we strongly encourage IAV surveillance with a multistate capture-recapture approach along the entire migratory flyway of mallards.

  • 2.
    Avril, Alexis
    et al.
    ONCFS, France.
    Letty, Jerome
    ONCFS, Direct Etud & Rech, F-34990 Juvignac, France.
    Leonard, Yves
    ONCFS, F-45370 Dry, France.
    Pontier, Dominique
    Univ Lyon .
    Exploration forays in juvenile European hares (Lepus europaeus): dispersal preludes or hunting-induced troubles?2014In: BMC Ecology, ISSN 1472-6785, E-ISSN 1472-6785, Vol. 14, article id 6Article in journal (Refereed)
    Abstract [en]

    Background: Movements of animals have important consequences, at both the individual and population levels. Due to its important implications in the evolutionary dynamics of populations, dispersal is one of the most studied types of movement. In contrast, non-permanent extra home-range movements are often paid less attention. However, these movements may occur in response to important biological processes such as mating or predation avoidance. In addition, these forays are often preludes to permanent dispersal, because they may help individuals gain cues about their surroundings prior to settlement in a new place. In the European hare, exploration forays occur predominantly in juveniles, the time at which most hares disperse. In France, the timing of dispersal also overlaps with the hare hunting period. However, the determinants of such behaviour have not yet been studied. Herein, we investigate whether these non-permanent explorations are dispersal attempts/preludes or, in contrast, whether they are triggered by other factors such as disturbances related to hunting. Results: Contrary to natal dispersal, we did not find strong male-bias in the propensity to engage in explorations. Exploration forays occurred less in juveniles than in adults and later in the season than natal dispersal. This was the case both for philopatric movements and for movements occurring after dispersal and settlement. These movements were also more likely to occur during the hare hunting period and the mating season. Conclusions: We suggest that explorations in hares are triggered by factors other than dispersal and that hares may respond to hunting disturbances. Overall, we emphasize the need to account for human-related predation risk as a factor driving space-use in harvested species.

  • 3.
    Bengtsson, Daniel
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Gunnarsson, Gunnar
    Kristianstad University.
    Elmberg, Johan
    Kristianstad University.
    Söderquist, Pär
    Kristianstad University.
    Norevik, Gabriel
    Ottenby Bird Observatory.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Safi, Kamran
    Max Planck Institute for Ornitholology, Germany ; University of Konstanz, Germany.
    Fiedler, Wolfgang
    Max Planck Institute for Ornitholology, Germany ; University of Konstanz, Germany.
    Wikelski, Martin
    Max Planck Institute for Ornitholology, Germany ; University of Konstanz, Germany.
    Olsen, Björn
    Uppsala University.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Movements, Home-Range Size and Habitat Selection of Mallards during Autumn Migration2014In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 9, no 6, article id e100764Article in journal (Refereed)
    Abstract [en]

    The mallard (Anas platyrhynchos) is a focal species in game management, epidemiology and ornithology, but comparably little research has focused on the ecology of the migration seasons. We studied habitat use, time-budgets, home-range sizes, habitat selection, and movements based on spatial data collected with GPS devices attached to wild mallards trapped at an autumn stopover site in the Northwest European flyway. Sixteen individuals (13 males, 3 females) were followed for 15-38 days in October to December 2010. Forty-nine percent (SD = 8.4%) of the ducks' total time, and 85% of the day-time (SD = 28.3%), was spent at sheltered reefs and bays on the coast. Two ducks used ponds, rather than coast, as day-roosts instead. Mallards spent most of the night (76% of total time, SD = 15.8%) on wetlands, mainly on alvar steppe, or in various flooded areas (e.g. coastal meadows). Crop fields with maize were also selectively utilized. Movements between roosting and foraging areas mainly took place at dawn and dusk, and the home-ranges observed in our study are among the largest ever documented for mallards (mean = 6,859 ha; SD = 5,872 ha). This study provides insights into relatively unknown aspects of mallard ecology. The fact that autumn-staging migratory mallards have a well-developed diel activity pattern tightly linked to the use of specific habitats has implications for wetland management, hunting and conservation, as well as for the epidemiology of diseases shared between wildlife and domestic animals.

  • 4.
    Bengtsson, Daniel
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Safi, Kamran
    Max Planck Institute for Ornithology, Germany;University of Konstanz, Germany.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Fiedler, Wolfgang
    Max Planck Institute for Ornithology, Germany;University of Konstanz, Germany.
    Wikelski, Martin
    Max Planck Institute for Ornithology, Germany;University of Konstanz, Germany.
    Gunnarsson, Gunnar
    Kristianstad University.
    Elmberg, Johan
    Kristianstad University.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Olsen, Björn
    Uppsala University.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Does influenza A virus infection affect movement behaviour during stopover in its wild reservoir host?2016In: Royal Society Open Science, E-ISSN 2054-5703, Vol. 3, no 2, p. 1-11, article id 150633Article in journal (Refereed)
    Abstract [en]

    The last decade has seen a surge in research on avian influenza A viruses (IAVs), in part fuelled by the emergence, spread and potential zoonotic importance of highly pathogenic virus subtypes. The mallard (Anas platyrhynchos) is the most numerous and widespread dabbling duck in the world, and one of the most important natural hosts for studying IAV transmission dynamics. In order to predict the likelihood of IAV transmission between individual ducks and to other hosts, as well as between geographical regions, it is important to understand how IAV infection affects the host. In this study, we analysed the movements of 40 mallards equipped with GPS transmitters and three-dimensional accelerometers, of which 20 were naturally infected with low pathogenic avian influenza virus (LPAIV), at a major stopover site in the Northwest European flyway. Movements differed substantially between day and night, as well as between mallards returning to the capture site and those feeding in natural habitats. However, movement patterns did not differ between LPAIV infected and uninfected birds. Hence, LPAIV infection probably does not affect mallard movements during stopover, with high possibility of virus spread along the migration route as a consequence.

  • 5.
    Bengtsson, Daniel
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Tailwind better than full tank? How weather and body condition affect departure decision in an autumn-staging migrantManuscript (preprint) (Other academic)
  • 6.
    Latorre-Margalef, Neus
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Georgia, USA.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Olsen, Björn
    Uppsala University.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    How Does Sampling Methodology Influence Molecular Detection and Isolation Success in Influenza A Virus Field Studies?2016In: Applied and Environmental Microbiology, ISSN 0099-2240, E-ISSN 1098-5336, Vol. 82, no 4, p. 1147-1153Article in journal (Refereed)
    Abstract [en]

    Wild waterfowl are important reservoir hosts for influenza A virus (IAV) and a potential source of spillover infections in other hosts, including poultry and swine. The emergence of highly pathogenic avian influenza (HPAI) viruses, such as H5N1 and H5N8, and subsequent spread along migratory flyways prompted the initiation of several programs in Europe, North America, and Africa to monitor circulation of HPAI and low-pathogenicity precursor viruses (low-pathogenicity avian influenza [LPAI] viruses). Given the costs of maintaining such programs, it is essential to establish best practice for field methodologies to provide robust data for epidemiological interpretation. Here, we use long-term surveillance data from a single site to evaluate the influence of a number of parameters on virus detection and isolation of LPAI viruses. A total of 26,586 samples (oropharyngeal, fecal, and cloacal) collected from wild mallards were screened by real-time PCR, and positive samples were subjected to isolation in embryonated chicken eggs. The LPAI virus detection rate was influenced by the sample type: cloacal/fecal samples showed a consistently higher detection rate and lower cycle threshold (Ct) value than oropharyngeal samples. Molecular detection was more sensitive than isolation, and virus isolation success was proportional to the number of RNA copies in the sample. Interestingly, for a given Ct value, the isolation success was lower in samples from adult birds than in those from juveniles. Comparing the results of specific real-time reverse transcriptase (RRT)-PCRs and of isolation, it was clear that coinfections were common in the investigated birds. The effects of sample type and detection methods warrant some caution in interpretation of the surveillance data.

  • 7.
    Latorre-Margalef, Neus
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. Univ Georgia, Dept Populat Hlth, Coll Vet Med, Southeastern Cooperat Wildlife Dis Study, Athens, GA 30602 USA.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Grosbois, Vladimir
    Int Res Ctr Agr Dev CIRAD UPR AGIRs, Anim & Integrate Risk Management, F-34398 Montpellier, France.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Bengtsson, Daniel
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Wille, Michelle
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Osterhaus, Albert D M E
    Erasmus MC, Dept Virol, Rotterdam, Netherlands.
    Fouchier, Ron A M
    Erasmus MC, Dept Virol, Rotterdam, Netherlands.
    Olsen, Björn
    Uppsala Univ.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Long-term variation in influenza A virus prevalence and subtype diversity in migratory mallards in northern Europe.2014In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 281, no 1781, p. Article ID: UNSP 20140098-Article in journal (Refereed)
    Abstract [en]

    Data on long-term circulation of pathogens in wildlife populations are seldom collected, and hence understanding of spatial-temporal variation in prevalence and genotypes is limited. Here, we analysed a long-term surveillance series on influenza A virus (IAV) in mallards collected at an important migratory stopover site from 2002 to 2010, and characterized seasonal dynamics in virus prevalence and subtype diversity. Prevalence dynamics were influenced by year, but retained a common pattern for all years whereby prevalence was low in spring and summer, but increased in early autumn with a first peak in August, and a second more pronounced peak during October-November. A total of 74 haemagglutinin (HA)/neuraminidase (NA) combinations were isolated, including all NA and most HA (H1-H12) subtypes. The most common subtype combinations were H4N6, H1N1, H2N3, H5N2, H6N2 and H11N9, and showed a clear linkage between specific HA and NA subtypes. Furthermore, there was a temporal structuring of subtypes within seasons based on HA phylogenetic relatedness. Dissimilar HA subtypes tended to have different temporal occurrence within seasons, where the subtypes that dominated in early autumn were rare in late autumn, and vice versa. This suggests that build-up of herd immunity affected IAV dynamics in this system.

  • 8.
    Tolf, Conny
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Wille, Michelle
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Haidar, Ann-Katrin
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Zohari, Siamak
    National Veterinary Institute.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Prevalence of avian paramyxovirus type 1 in Mallards during autumn migration in the western Baltic Sea region2013In: Virology Journal, ISSN 1743-422X, E-ISSN 1743-422X, Vol. 10, article id 285Article in journal (Refereed)
    Abstract [en]

    Background: Newcastle disease virus (NDV) is the causative agent of the Newcastle disease, a severe disease in birds associated with substantial economic losses to the poultry industry worldwide. Sweden is situated along the Western European waterfowl flyway and applies a non-vaccination policy combined with directives of immediate euthanisation of NDV infected flocks. During the last decades there have been several outbreaks with NDV in poultry in Sweden. However, less is known about the virus prevalence in the wild bird population including waterfowl, a well-established reservoir of avian paramyxovirus type 1 (APMV-1), the paramyxovirus serotype that include pathogenic NDV. Methods: The survey constituted of 2332 samples from Mallards (Anas platyrhynchos), trapped in the southern part of Sweden during autumn migration in 2010. These samples were screened for APMV-1 by real-time reverse transcription PCR, and viral strains from positive samples were isolated and characterized by sequence analysis of the fusion gene and by phylogenetic analysis. Conclusions: Twenty of these samples were positive for APMV-1, hence a virus prevalence of 0.9% (95% Confidence Interval [95% CI]=0.54%, 1.35%). The highest APMV-1 prevalence was detected in juvenile Mallards sampled in November (n=887, prevalence 1.24% ([95% CI])=0.67%, 2.24%). Sequence analysis and evaluation of phylogenetic relatedness indicated that isolated APMV-1 strains were lentogenic, and phylogenetically most closely related to genotype Ib strains within the clade of class II viruses. The sampling system employed enabled us to follow APMV-1 infections and the shedding of one particular viral strain in one individual bird over several days. Furthermore, combining previous screening results with the APMV-1 detections in this study showed that more than 50% of Mallards that tested positive for APMV-1 RNA were co-infected with influenza A virus.

  • 9.
    van Toor, Mariëlle L.
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Wu, Guohui
    SAS Inst Inc, USA.
    Holan, Scott H.
    Univ Missouri, USA.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    As the Duck Flies-Estimating the Dispersal of Low-Pathogenic Avian Influenza Viruses by Migrating Mallards2018In: Frontiers in Ecology and Evolution, E-ISSN 2296-701X, Vol. 6, article id 208Article in journal (Refereed)
    Abstract [en]

    Many pathogens rely on the mobility of their hosts for dispersal. In order to understand and predict how a disease can rapidly sweep across entire continents, illuminating the contributions of host movements to disease spread is pivotal. While elegant proposals have been made to elucidate the spread of human infectious diseases, the direct observation of long-distance dispersal events of animal pathogens is challenging. Pathogens like avian influenza A viruses, causing only short disease in their animal hosts, have proven exceptionally hard to study. Here, we integrate comprehensive data on population and disease dynamics for low-pathogenic avian influenza viruses in one of their main hosts, the mallard, with a novel movement model trained from empirical, high-resolution tracks ofmallardmigrations. This allowed us to simulate individualmallard migrations from a key stopover site in the Baltic Sea for the entire population and link these movements to infection simulations. Using this novel approach, we were able to estimate the dispersal of low-pathogenic avian influenza viruses by migrating mallards throughout several autumn migratory seasons and predicted areas that are at risk of importing these viruses. We found that mallards are competent vectors and on average dispersed viruses over distances of 160 km in just 3 h. Surprisingly, our simulations suggest that such dispersal events are rare even throughout the entire autumn migratory season. Our approach directly combines simulated population-level movements with local infection dynamics and offers a potential converging point for movement and disease ecology.

  • 10.
    Wille, Michelle
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. CIRAD, F-34398 Montpellier, France.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Schager, Anna
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Larsson, Sara
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Borg, Olivia
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Olsen, Björn
    Uppsala Univ.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Temporal dynamics, diversity, and interplay in three components of the virodiversity of a Mallard population: Influenza A virus, avian paramyxovirus and avian coronavirus2015In: Infection, Genetics and Evolution, ISSN 1567-1348, E-ISSN 1567-7257, Vol. 29, p. 129-137Article in journal (Refereed)
    Abstract [en]

    Multiple infections, or simultaneous infection of a host with multiple parasites, are the rule rather than the exception. Interactions between co-occurring pathogens in a population may be mutualistic, competitive or facilitative. For some pathogen combinations, these interrelated effects will have epidemiological consequences; however this is as yet poorly incorporated into practical disease ecology. For example, screening of Mallards for influenza A viruses (IAV) have repeatedly revealed high prevalence and large subtype diversity in the Northern Hemisphere. Other studies have identified avian paramyxovirus type 1 (APMV-1) and coronaviruses (CoVs) in Mallards, but without making inferences on the larger viral assemblage. In this study we followed 144 wild Mallards across an autumn season in a natural stopover site and constructed infection histories of IAV, APMV-1 and CoV. There was a high prevalence of IAV, comprising of 27 subtype combinations, while APMV-1 had a comparatively low prevalence (with a peak of 2%) and limited strain variation, similar to previous findings. Avian CoVs were common, with prevalence up to 12%, and sequence analysis identified different putative genetic lineages. An investigation of the dynamics of co-infections revealed a synergistic effect between CoV and IAV, whereby Coy prevalence was higher given that the birds were co-infected with IAV. There were no interactive effects between IAV and APMV-1. Disease dynamics are the result of an interplay between parasites, host immune responses, and resources; and is imperative that we begin to include all factors to better understand infectious disease risk. (C) 2014 Elsevier B.V. All rights reserved.

  • 11.
    Wille, Michelle
    et al.
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Tolf, Conny
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Avril, Alexis
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. CIRAD, Campusinternational de Baillarguet, Montpellier 34398, France.
    Latorre-Margalef, Neus
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Wallerström, Sofie
    Karolinska institutet.
    Olsen, Björn
    Uppsala universitet.
    Waldenström, Jonas
    Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.
    Frequency and patterns of reassortment in natural influenza A virus infection in a reservoir host2013In: Virology, ISSN 0042-6822, E-ISSN 1096-0341, Vol. 443, no 15, p. 150-160Article in journal (Refereed)
    Abstract [en]

    Influenza A viruses (IAV) can dramatically alter both genotype and phenotype at a rapid rate as a product of co-infection and reassortment Avian IAV exhibit high levels of phylogenetic incongruence, suggesting high levels of reassortment in the virus reservoir. Using a natural-experimental system, we reconstructed relationships amongst 92 viruses across 15 subtypes from 10 Mallards in an autumn season. Phylogenetic analyses estimated that 56% of the isolated viruses were reassorted. Network analysis demonstrated different patterns of reassortment and limited exchange of segments between primary and secondary infections. No clear patterns of linkage between segments were found, and patterns within a season were likely the consequence of continued introduction ofnew constellations, high viral load and diversity in the wild bird reservoir, and co-infections. This is the first IAV study to implement multiple tools available for elucidating factors governing reassortment patterns in naturally infected Mallards.

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