Seabirds and flu, a review

A small murre colony on Cabot Island, Canada.

[This post is by Michelle Wille, postdoctoral researcher at Uppsala University]

For those who have visited a seabird colony, you would know that it is a loud and crowded place, with large swaths of the colony covered in guano. It literally stinks of bird poo. If you were to imagine a good host for a virus that is transmitted by the fecal oral route, one could imagine that these conditions would be excellent for transmission. A virus, such as the influenza A virus (IAV).

 

This virus is one of the most important and well-studied avian viruses, especially in its reservoir hosts, the dabbling ducks. However, for seabirds – the majestic creatures that roam the oceans – no real synthesis has been published despite close to 50 years of surveillance. In fact, when I started working on IAV in seabirds, we knew very little about the presence and prevalence of influenza in this group of birds. What we did know was that seabirds were being sampled for influenza – in fact, most bird groups were being sampled for IAV following the highly pathogenic H5N1 outbreaks after 2005 – but we didn’t actually know how seabirds fit into the ecology of influenza. Are they infected? Are some seabirds more important than others? Do they follow similar patterns to ducks or gulls? Are their viruses unique, or more similar to duck or gulls?

 

Antarcric Tern

Antarctic tern

We set out to collate the existing knowledge on IAV in seabirds – a diverse collection of species and are best defined through their shared propensity to spend portions of their lives at sea – and pulled together as much surveillance data as possible from publications and influenza databases to try to evaluate sampling effort in seabirds, and which species play a role in IAV ecology. This review was just published in the journal Avian Diseases. It turns out, scientists have sampled a large number of seabirds over the last 50 years: 41,828 samples from 98 species, spanning 14 avian families in 6 orders. This may seem like a lot of samples, but if broken down it equals only 8.5 samples per species per year. To put it in perspective, from our sampling site in Sweden, 22,229 samples were collected from Mallards between 2002-2009, and it is samples sizes like these that allow us to make stronger inferences on IAV ecology.

 

While this illustrates the lack of effort overall, some seabirds have received more effort and attention. Terns as a group are heavily sampled, although sporadically rather than systematically. Terns are interesting as the first confirmed outbreak of highly pathogenic influenza in wild birds occurred in Common Terns (Sterna hirundo) in South Africa back in 1961. Despite very few isolations of viruses, serology suggests circulation of IAV in terns and noddies and a diversity of virus subtypes – most recently highlighted in the Indian Ocean system. Most interesting, perhaps is the compelling evidence suggesting that Murres/Guillemots (Uria sp.) are hosts for IAV. Research to investigate IAV in murres dates back to the 1970s, and interest in these birds has been renewed with increased sampling effort in the past 10 years. These birds are piscivorous, limited to the northern Holoarctic where they breed predominantly on islands, often on steep cliffs. Within all the seabird groups, the greatest number and diversity of viruses come from murres, with viruses isolated across their range – Russia, Sweden, Greenland, Newfoundland (Canada), Nunavut (Canada), Alaska (USA), and Oregon (USA). Unfortunately there is rather limited serological information in Common and Thick-billed Murre, which would provide a more long-term assessment of influenza dynamics.

 

 

COMU

A few other species/groups have large enough sample sizes to estimate IAV prevalence with confidence, but serology, despite small sample sizes, indicates IAV presence in most seabird species tested. However, more focused work is required to better assess these species as hosts. Regardless, if you are interested in the IAV status of the seabirds you work on – sampling effort and IAV results are presented for all 98 species.

 

concept

What is the role of seabirds in the epidemiology of low-pathogenic avian influenza?

What was a surprise for us, as we were completing this review, was how little we could say about the role of seabirds in the ecology of seabirds due to limitations in sampling. There is clearly a space to fill for an aspiring IAV researcher. If you want to sample for IAV and be able to draw some conclusions – here are some things to think about:

 

  1. Influenza A in birds is seasonal. Some months the prevalence is high (up to 30%) and some months it is low (>0.00001%). While seabirds are logistically hard to access, temporal and repeated sampling is key.

 

  1. Within an individual, the period of shedding live virus is very short. While longer periods have been detected (up to 14 days), usually birds shed viruses for less than 7 days. This highlights the importance of serology, or assessing the antibody prevalence in a population. This allows us to ascertain whether the population has been infected by IAV in the past, and therefore, whether it is a population to target (if positive).

 

  1. Seabird colonies may have many species, and it is tempting to take a few samples from each species present. Low sample size however limits the detection probability. For example, if prevalence of IAV is about 1% in the population, you need to take well over 100 samples to have a 95% probability of detecting the virus. Putative prevalence of IAV in seabirds is in this 1% range.

 

  1. Maintaining “cold chain” is key. Seabird colonies are logistically hard to sample, and dragging a -80C freezer or vapour shipper may just not seem to be worth the effort. But, RNA viruses degrade rather rapidly, and swaths of negative samples may be false negatives due to poor sampling handling. While it is speculation, perhaps the reason that we are starting to be more successful at isolating influenza from Antarctic Penguins is an improvement in cold chain (who would have through it would be difficult to keep samples at a constant temperature of -80C in Antarctic!).

 

I feel privileged to be writing this piece after recently spending a week working in a Murre colony in Sweden. Seabird colonies really are the best places to be – serene beauty on the steep, the smell of guano-ladened cliffs on (remote) islands, with the flutter of murre wings and peeping of recently hatched murre chicks.

Link to the article:

Andrew S. Lang, A.S., Lebarbenchon, C., Ramey, A.M., Robertson, G.J., Waldenström, J.& Wille, M. 2016. Assessing the Role of Seabirds in the Ecology of Influenza A Viruses. Avian Diseases 60(1s):378-386.

 

Penguins

Adelie and Gentoo penguins doing their thing.

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