The duck, the seed, the distance – mallards as seed dispersers

A seed disperser in action (Flickr, USFSW Mountain Praire CC BY 2.0)

(This post is by Mariëlle van Toor, on Twitter as @mlvantoor)

Most of the stories on this blog somehow relate to birds (particularly ducks) and pathogens (most often avian influenza viruses, or AIV). Throughout the years, we have established that ducks are quite good at transporting AIV during their daily movements, and even migration. But viruses are not the only thing that ducks are able transport! Specialist wetland plants, which inhabit discrete habitats that are often not connected by waterways, have usually very little opportunity for (long-distance) dispersal that would allow them to colonise new wetlands. Dabbling ducks such as the mallards forage on all kinds of seeds, which they crush in a specialised organ called gizzard to make them easier to digest. However, seeds often escape from the gizzard unharmed. These seeds will be excreted by the ducks rather than digested, and can grow into mature plants. By transporting the seeds of wetland plants in this way, ducks could fill an ecologically important role.

But just how much could migratory ducks such as mallards contribute to seed dispersal? This was the question that our collaborator Erik Kleyheeg, then a PostDoc at the Max Planck Institute for Ornithology, approached us with. Erik (now also known as the “Teal man”) had already accumulated a wealth of knowledge on mallard seed dispersal during his PhD, and had collected spring migratory tracks of mallards wintering at Lake Constance. Combined with the extensive ring recovery data set from the same population of mallards, the duration of seed passage through the gut, and the models we previously applied for our virus dispersal paper (see post here), we developed our “comprehensive mallard seed dispersal model” that is now published in Frontiers in Ecology and Evolution.

But what does comprehensive mean in terms of mallard seed dispersal? For that we need to know what previous attempts at modelling seed dispersal by mallards during migration looked like. Often, previous studies have estimated seed dispersal distances during bird migration by multiplying distributions of gut retention time with the flight speed of birds. But neither do ducks fly in a straight line, nor do they fly uninterruptedly between their wintering and breeding areas. We thus need to account for staging behaviour and specifics of the migratory flight, and consider dispersal during the different stages of migration.

The black line shows the curve describing the retention of seeds in a mallard’s gut. Most seeds will be excreted soon after ingestion (depending on seed size), but the long tail could enable ducks to transport seeds over long distances both during migratory legs and staging periods.

Our model includes both seed dispersal during the actual migratory flight, and during the time that ducks are staying at stopover sites.

Another important aspect is that we need to account for when individuals stop foraging. Do they eat seeds right up until the start of a migratory flight, or do individuals fast prior to migration to avoid carrying around any extra weight? As the answer to this question is not satisfactorily resolved yet, we decided that our model should be able to account for fasting time. For our paper, we considered three scenarios – no fasting, short fasting (1 hour prior to migration), and long fasting (12 hours prior to migration) – to understand how fasting would affect seed dispersal. As soon as we better understand the behaviour of pre-migratory fasting in ducks, however, we can feed any number into the model for more specific (and realistic) predictions.

The duration of pre-migratory fasting affects potential dispersal distances quite substantially. Above you can see how short and long retention times (for small and large seeds, respectively) are affected by fasting duration.

Finally, all seed dispersal is to no end if seeds are not transported to habitat for suitable for germination. For wetland plants, that obviously means transport to other wetlands. While all other components of the seed dispersal kernel derived from our model should be transferable to other mallard populations, the availability of wetlands along the migratory corridor were specific to this population. We calculated the probability of dispersed seeds to end up in wetland habitat for both staging mallards, which can be found in wetlands most of the time, and for migratory individuals, for which we used the Global Lakes and Wetlands Database (GLWD). Our summary map for wetland availability already shows that it is not very likely for a seed dispersed by an actively migrating mallard to be deposited in a wetland:

Most migratory mallards wintering at Lake Constance migrate along a N-E corridor. The highest concentration of wetland area lie towards the East and North East.

All this taken together, the question is: How good are mallards as seed dispersers? You won’t like the answer: it depends! Theoretically, mallards are amazing at transporting seeds – if they don’t fast before starting migration. If mallards foraged right up until migration, they could transport a large part of the swallowed seeds over hundreds of kilometers, and many of them would end up in suitable habitat during the first stopover period. But the duration of pre-migratory fasting hugely influences dispersal distances, and in the 12 hour scenario, many seeds were already excreted prior to migration. But even then, some seeds can be transported over exceptional distances.

These are the final seed dispersal kernels predicted from our model, shown for short and long retention times, and three different scenarios of pre-migratory fasting. The upper row shows the general probability of seeds being dispersed over distances up to 950 km (the general prediction), whereas the lower row shows the probability of seeds being dispersed into suitable habitat (the prediction specific to Lake Constance mallards).

In conclusion, migratory ducks such as mallards likely play an important role for the short- and long-distance dispersal of wetland plants, both during periods of migration and residency. But, as always, there are more questions to be answered before we can say for sure.

Link to the paper:

Kleyheeg, E., Fiedler, W., Safi, K., Waldenström, J. & Wikelski, M. & van Toor, L. M. 2019. A comprehensive model for the quantitative estimation of seed dispersal by migratory mallards. 2019. Frontiers in Ecology and Evolution 7:40 [10.3389/fevo.2019.00040]

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On the steppes of Askania Nova

The circles are the parts of the field that are irrigated, while the drier ‘corners’ are planted with different crops.

Southern Ukraine. From Zaporizhza to Askania Nova we pass field after field on the straight (but bumpy) road. The fields are huge, bigger than any fields I’ve seen. This is farming on the industrial scale. Once upon a time this was the river bed of one of Europe’s largest river, which deposited a thick layer of soil perfect to till. But it is dry, and without pumping water from Dnepr most of the fields would be steppe.

Johannes Rydström and I have traveled here to meet with Denys Muzika and his team of ornithologists and virologist. Over the course of a week, we try and catch ducks to equip them with GPS loggers that allow us to study migratory connectivity and influenza A virus dispersal. Just a few weeks earlier I was doing similar work in Bangladesh, and the contrasts in temperature, landscape and number of people couldn’t be larger.

Our base is Askania Nova, a pristine steppe reserve in the southern part of the country. It is a popular tourist destination and the site has a very ambitious zoo with large ungulates and birds, and a huge park with a collection of diverse trees. It is a gem and as a birdwatcher the steppe birds are amazing to see, with a constant background of singing Calandra larks.

Our team scouted different wetlands in the area and we tried to capture birds most nights using mist nets and duck calls. Depite our efforts and some amazing wetlands, we were not as successful as we had hoped. But at the end of the trip we can note 9 mallards equipped with loggers, of which one directly migrated to Russia. A big part of the trip was to connect and build for the future, because this is a site of strategic importance for influenza and duck research, on the gateway to Europe on the Caspian/Black Sea flyway.

We will be back.

A male mallard is about to be equipped with a logger. This bird is currently in southern Ukraine. Photo Johannes Rydström.

Several nights we worked in a beautiful steppe lake, putting up mist nets to catch ducks. This is Denys in action. Photo Johannes Rydström.

Sweden-Ukraine Duck Team (Denys, Sasha, Raysa, Jonas and Kolja) Photo Johannes Rydström.

This is me!

Tanguar Haor – a legendary wetland

IMG_0414There’s no business, like duck business

This spring I have been going places. First Bangladesh, and then Ukraine. Both trips connected by ducks, and the hopes of using telemetry to infer migratory connectivity of waterfowl populations and the transmission risk of avian influenza viruses.

Together with our colleagues at IUCN Bangladesh we spent some magnificent weeks in the wetlands of northeastern Bangladesh catching wintering ducks. I am writing up a longer piece of this trip for Birdlife Sweden’s magazine Vår fågelvärld which I hope to share with you in a couple of months. In the meantime, I’d like to refer you to an excellent article by Abida Rahman Chowdhury, a journalist from The Daily Star who visited us in the field in Tanguar Haor – the gem of wetlands in the north. Please read it on this link.

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

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