As the duck flies: Avian influenza virus and migratory mallards

For a pathogen to survive it has to find new hosts to infect. This may sound simple, but if you consider the entangled mesh that is the biology of a host species you realize that there are plenty of ways that things can go wrong, stopping the chain of transmission. First of all, the harm the pathogen incurs on its host – the virulence – needs to be balanced between being too low – the infection will be cleared before any transmission opportunities have occurred –  or too high, so that it causes the demise of the host before transmission can take place. Second, the pathogens must overcome the hurdles of moving from one host to the next, be it in water, air or through the bite of an arthropod vector. And third, it has to overcome the fact that most hosts are not sedentary, but move varying distances in response to changes in the environment they inhabit. Finally, it needs to be able infect the new host and evade the immune system to establish infection. Not an easy feat, but something that is happening all the time in the world of viruses, bacteria, fungi, parasites and their hosts.

In the avian influenza field, the realization of the importance of bird migration in the epidemiology has a long history but we haven’t really been able to address it in the required detail. Most studies have addressed the process at the population level, inferring movements either from ring recoveries or from virus phylogenetic perspectives. If you have followed what we do, it will not come as a surprise that we are interested in both influenza viruses and bird migration. A longstanding goal for us has been to integrate virology and movement ecology to better understand the epidemiology of avian pathogens. This is where it gets exciting, as the technology needed for these types of studies are available. Last year we deployed loggers on migrating mallards at our main study site, the Ottenby Bird Observatory on the island of Öland in SE Sweden, and followed them during migration as a part of the H2020 program DELTA-FLU.

We programmed the loggers to record GPS-positions in bursts, hoping to retrieve as much data as possible during active flight. From the flight data we extracted the metrics of flight: how does a mallard migrate – how fast, how high, and in which direction? And how do these parameters change during the flight? These metrics formed the basis for a Mallard Migration Simulator with which we could simulate different types of migrations, based on the normal flight behaviors of mallards.

The next step was to use the ring recoveries retrieved from the study site over the last 50 years to get realistic headings of migratory flights. Finally, we introduced individual-level epidemiological parameters from our study populations and built classical SIR-models. Combined, this allowed us to look at the likelihood that a bird that migrated was infected with low-pathogenic avian influenza, and that it maintained infection during migration, controlled by season, age of birds and other factors that could contribute. The resulting data can be transformed into a risk map for transmission.

I am very pleased with this approach, and think it is a novel way of analyzing this type of data. The next step, of course, is to consider such models for highly-pathogenic avian influenza viruses on larger spatial scales. We are collecting tracks of four species of ducks in different parts of Eurasia and hopefully we will be able to make realistic models of virus dissemination among migratory ducks in a flyway perspective.

Link to the paper:

van Toor, M.L., Avril, A., Wu, G., Holan, S.H. & Waldenström, J. 2018. As the duck flies – estimating the dispersal of low-pathogenic avian influenza viruses by migrating mallards. Frontiers in Ecology and Evolution 6:208. doi: 10.3389/fevo.2018.00208

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How to infect your duck, with science

How to infect a duck?

A critical parameter for the spread of a pathogen is the mode of transmission. Some pathogens have evolved to use mosquitoes or ticks as transmission vectors; others rely on direct contact, such as via body fluids during sex, and a score of pathogens travel by air, water or soil to reach the next host. Which route that is optimal depends on the interplay between the pathogen, the host(s) and the environment they occupy.

If we think about ducks, it makes sense to consider water as an effective medium for pathogen transmission. This indeed the case for several duck pathogens, and perhaps most notoriously for low-pathogenic avian influenza viruses. In ducks these viruses are common, causing mild gastrointestinal infections, and infected virus particles are shed in high numbers in feces. The conventional wisdom has been that the fecal-oral infection route is the most important, strengthen by the feeding habits of dabbling ducks where they skim the surface for food items, thereby exposing themselves for newly excreted viruses from their ducky friends.

But if you look yonder, at the ducks bobbing around in the pond, you will notice that they do other things as well. Of course, they dabble their bills in the surface waters, but they occasionally stretch the head and neck down to nibble at food stuff further down in the water. To keep the plumage nice and clean – and their bodies dry – they spend a significant proportion of their time carefully preening their feathers.

Such observations have resulted in alternative infection mode hypotheses, but until now we haven’t been able to disentangle them. In a seminal publication, Wille and co-workers at Uppsala University tested to what extent low-pathogenic avian influenza viruses can infect mallard ducks via the process of cleaning their feathers, or via the rear end, in a process called ‘cloacal drinking’. The drinking part refers to that when pressures are posed when ducks poo, it may create a vacuum through which a little volume of water enters the cloaca, which if containing influenza virions may cause an infection in the lower intestinal tract, bypassing the more traditional mechanism of swallowing viruses.

The paper is essentially an ‘how to infect your duck’ guide, complete with some clever appliances and boxes, and rounds of disinfections, to clearly separate the different modes of infection. And, yes, there are indeed many ways to infect a duck, as both preening and cloacal drinking also resulted in infections. Overall It is time for broadening our view of possible infection routes for flu, and other pathogens, especially those that are transmitted through water.

Link to the paper:

Wille, M., Bröjer, C., Lundkvist, Å. & Järhult, J. 2018. Alternate routes of influenza A virus infection in Mallard (Anas platyrhynchos). Veterinary Research 49:110

 

Ducks lost and found

Waiting at the shoreline (Flickr CC BY 2.0)

Tracking birds is a rollercoaster ride between excitement and disappointment. Even though the technology is improving rapidly, some loggers will fail anyway, some birds will be taken by a predator, and some birds just don’t do all the exciting things you hoped they would. But on the other hand, when everything works you get extremely detailed knowledge about the behavior of individual birds across the annual cycle.

Given this, and the cost of each logger, there is always that moment on the shoreline. You see the bird (in our case a duck) fly, very rapidly away and the question of what will happen next forms in your mind. Will we learn anything about its life, will we see it again? Have we interfered too much in its life?

Over the years we have learned a bit on the rough life of ducks. A number of ducks have been shot by hunters, either reported by the hunters or detected by logger movements in cars and fixes on farmsteads. Quite a few we believe have been killed by predators, including a northern pintail that was taken by a goshawk within two hours of deployment and a mallard eaten by a fox in eastern Germany. On top of that we have adverse weather events, such as cold spells and blizzards that take they their toll on wintering birds.

One particular problem is when a bird reaches an area where the logger no longer has connection and can not send data. The bird is gone, vanished from the map. This is especially evident for two of our study species, the Eurasian wigeon and the northern pintail. Both species breed in large numbers on the tundra, far away from human settlements, in areas where mobile phones do not work. Thus, there comes a time when the signal is lost, and you can only hope the bird will return and send data again sometime later.

For our wigeons, we had seven birds that were lost this summer: Nicola in Murmansk, Sarah in eastern Finland, Fitzwilliam in the Pechora river in Russia, and Michelle, Sita, Ellinor and Pär east of the Ural mountains. But in the last week we have reconnected with Sarah in Archangelsk and Fitzwilliam in Estonia, and hopes are we will get reconnected with some of the others.

Until then we are waiting at the shoreline.

Fitzwilliam the wigeon: he once was lost, but now am found

Linnaeus goes Motus

It is already mid-October, but the weather is still mild for the season, especially so the last couple of days. Today we took advantage of the sunny autumn day and headed up on the roof. And what splendid scenery there is on top of the new university building! You can see tens of kilometers in each direction and have a clear view of the strait of Kalmar. A perfect spot to place our new MOTUS antennas.

And what is a Motus antenna, you may ask? Good question. The Motus Wildlife Tracking System is a collaborative research network that uses coordinated automated radio telemetry arrays to study movements of small animals. Or simply put: you can equip birds with mini radio transmitters and listen for them with large radio antennas. And by placing many antennas in a flyway of birds, you can follow the birds during migration. This is a big thing in North America, and just recently have started to become more common in Europe. If you look at the maps below you see that the towers currently are focused to the Wadden Sea region, but with occasional towers elsewhere. Together with Ottenby Bird Observatory and Lund University we are now building a network of Motus towers on the island Öland.

Compared to other tracking techniques, Motus has the benefit of really, really small loggers – all the way down to 0.2g. This means you can put them on smaller birds compared to other types of loggers, and study migration of warblers, thrushes, swifts and waders. And the more towers the better, as all towers can detect all loggers and forward the data to the right project. Pretty nice! Thus, today we added a new tower to the system.

 

Duck (and virus) movements from afar

A wigeon track on the undulating tribituary of the Pechora river

Before I was a researcher, I was a birder. I spent my free time either birding, or thinking about birds. And my favorite place was Ottenby Bird Observatory. This is where my formative years took place and where I made friends for life. A focus point in my existence to this day. I spent countless mornings ringing birds at the observatory. Sleep deprived, sustained by coffee, sandwiches and tobacco we young ringers often talked about what would happen with the birds we released. Where would they go, what would they do? We marveled about the epic journeys they would undertake, connecting distant parts of the globe.

Sometimes we got answers, for one benefit of ringing is that the rings transform birds into individuals, and hence make possible to follow if they are trapped again, resighted or found dead. The downside is that these are all rare events, especially for smaller birds. For instance, the chance of getting a ring recovery of a willow warbler on wintering grounds in East Africa is very low, somewhere around 1 out of 100,000 ringed birds. For other birds like the mallard, the chance of a recovery is closer to 10% – a considerable difference. In any case, the information you get is limited and usually shown as a dot on a map.

But times have changed. I am older, greyer and possible wiser, a professor working with bird borne infections (but not birding as much as I would like to). I am still very interested in the question of where birds go, and what they do. Fortunately, tracking technology has taken giant leaps and we can now do studies that were unheard of when I was a young ringer. In recent years, my laboratory has been involved in studies investigating movement behavior of mallards. Together with Martin Wikelski’s team in Constance, we have looked at home range sizes and habitat selection of mallards during migratory stopovers, tested the hypothesis that influenza A virus infection impairs movements of mallards, and even made translocation experiments between Sweden and Germany to repeat Perdeck’s classic starling study. We have used Argos loggers, radio-frequency loggers and GSM-loggers, and for each study the loggers have become better and lighter and data ever more detailed.

Right now, we are a part of DELTA-flu, a Horizon2020 EU-project with several European partners. Our role is to investigate the migratory connectivity of waterfowl in Eurasia in light of HPAI virus transmission. Can we use loggers to answer the question about possible routes of virus transmission across continent?

An urban mallard in Roskilde, Denmark, presently hanging out on the Roskilde Festival camping site

The loggers we use come from the company Ornitela in Lithuania, and weigh 10, 15 or 25g depending on which duck species we target. The general rule of thumb is that a logger shouldn’t weigh more than 3% of the bird’s mass, as not to impair it unnecessarily. These loggers are little marvels; they transfer data via the mobile phone network and can be programmed remotely. So far we have deployed loggers in Sweden, Lithuania, Netherlands and Georgia, and are planning to work in Ukraine, South Korea and Bangladesh. We are also waiting for the next leap in telemetry: the ICARUS project onboard the International Space Station. With this technology, loggers may reach 2.5g and hence be put on a larger range of species. What all these loggers do is to provide a real-time window into birds’ movements: Where they are and what they are doing, sometimes even what they avoid or what caused their deaths. We can follow the lives of ducks in great detail.

There is a veritable flood of data, with more than one million GPS points collected already. It is easy to get lost in time just watching the latest whereabouts of the tagged ducks, from the tundra regions east of the Ural mountains to a gravel pit outside Bremen. I hope to write here more frequently, because there is a lot of exciting stuff happening in the lab at the moment – until then, have fun!

The art of the Teal

The life of teal is a life on the wing. It is the smallest dabbling duck in the Boreal zone, but in terms of migration it covers huge distances from breeding waters to the non-breeding areas far, far away. The same bird can spend time in an oligotrophic lake in Russia during breeding, a brackish Baltic Sea lagoon or a tidal mudflat in the Atlantic coast during autumn, and a rich river delta in the Mediterranean in winter – and some individuals even straddle over into North Africa for a dabble. It takes a lot of adaptability to switch between such vastly different habitats, and at the same time avoid becoming dinner of arial predators and human hunters.

This book – The Teal by Matthieu Guillemain and Johan Elmberg published in 2014 – is part of a long tradition of monographs in ornithology, and a must for everyone with love for ducks. It’s clear from the writing that the authors hold their study species dear, and each part of the annual cycle is covered in well-written informative chapters.

Because of hunting, ducks have long been a focus of research and there’s a huge body of literature on many aspects of duck ecology. However, it is not easy accessible, either because it is old, or that it has been published in journals with a narrow scope. Here the authors have done a massive job to summarize tons of hard-to-get information in text, as well as tables and appendixes. Although most readers will not spend too much time on the appendixes, they serve as reference when you need it. For instance, if you want to know the helminth fauna detected in Teal, you can peruse appendix 8 – a full 7 pages of wormy stuff, or for a list of food items turn to appendix 6.

Although the book is written in the scientific tradition and heavily referenced, it is still a fairly easy read with clear chapter distinctions and a number of boxes for specific questions. You get to know both the Eurasian Teal and the North American sister species Green-winged Teal – which are extremely similar in apperance and ecology, but with rather different research history. The book devotes one chapter to distribution and numbers, one to  movements and migrations, one to foraging and diet and one to breeding ecology. From there the book turns to mortality, demography, harvesting and conservation, before ending in a list of priorities for future research.

The teal is facinating bird and The Teal is a very good book. When reading it, it struck me how much I have yet to learn even though I have studied ducks professionally for several years. My main study species is the mallard, which although bigger and not as migratory share many traits with the teal, and knowledge presented in this book is valuable for all dabbling ducks. My largest knowledge gaps was the breeding and foraging ecology parts, and I am grateful for filling those by reading the book. But there are so many other aspects of teals that are facinating, including the apperant ease of long-distance migration despite generally not putting on large food reserves, or the intricate pair forming and sex life of ducks – and the very large hunting bags and their impact on population demography and numbers.

Thus, this book fills two purposes: as a general read for anyone interested in ducks, and a specialized reference book for researchers. It was published in 2014 and if you haven’t bought it yet, you should. Especially, I think this book is an essential read if you’re into avian influenza, to widen the horizon of the ecology of one of the virus’ main hosts. An increased understanding on the life history of dabbling ducks would go a long way to clear some misunderstandings that the field is laden with.

A pair of American Wigeons are about to land next to a pair of Eurasian Wigeons and mr and mrs Green-winged Teals.