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Research We will investigate the role of wild migratory birds in the transmission of highly pathogenic avian influenza (HPAI) H5N1 and we will determine the precise migratory routes and use of Asian stopover areas by Alaska-breeding Bar-tailed Godwits.
Surveillance Field surveillance sampling will target HPAIH5N1 and non-H5N1 viruses in Alaska and assess baseline levels of AI viruses in populations of shorebirds that migrate between Asia and Alaska.
Justification and Background Wild migratory birds have been implicated in the transmission of highly pathogenic avian influenza (HPAI) H5N1 across long distances and between continents (Ducatez et al. 2006). However, the extent to which migratory birds contribute to avian influenza outbreaks is still unknown (Muzaffar et al. 2006). Research is needed to identify routes whereby wild birds that are infected with HPAI H5N1 could carry the virus into North America. Research is also needed to determine if infected wild birds transmit the virus to conspecifics or to other species during their tenure in North America. Recent recommendations by virology and health experts (e.g., FAO 2006) advise ornithologists to focus research on describing basic life history parameters (e.g., precise migration routes, important congregation sites) of those migratory waterbirds that are at risk for HPAI infection. In particular, experts point to the need to understand the timing and routes used by migratory waterbirds in relation to patterns of AI distribution in poultry and wildlife. Such information is needed to design effective AI monitoring strategies, develop risk assessments, and predict future outbreaks of HPAI H5N1.
Several populations of Alaska-breeding shorebirds spend weeks or months of their annual cycle in Southeast Asia, often in habitats and areas utilized by poultry, and presumably in areas of H5N1 outbreaks. Other populations of shorebirds mix with birds from Southeast Asia on Siberian breeding areas before migrating to post-breeding areas in Alaska. These migration patterns place 10 populations of shorebirds in Alaska at relatively high risk among waterbirds for becoming infected with HPAI H5N1 and subsequently carrying it into North America (Alaska Interagency HPAI Bird Surveillance Working Group 2006). In this study, we plan to describe in detail the migration behavior of one high-risk species, the Bar-tailed Godwit (Limosa lapponica), and to continue to sample all Asia-Alaska shorebird migrants either by design (see below) or opportunistically.
Populations of shorebirds in Alaska that are considered high risk candidates for spreading HPAI H5N1 include (in order of perceived risk): Dunlin (Calidris alpina arcticola), Sharp-tailed Sandpipers (Calidris acuminata), Bar-tailed Godwits, Ruddy Turnstones (Arenaria i. interpres), Pectoral Sandpipers (C. melanotos), Long-billed Dowitchers (Limnodromus scolopaceus), Red Knots (Calidris canutus rogersi and C. c. roselaari), Rock Sandpipers (C. ptilocnemis tschuktschorum), Pacific Golden-Plovers (Pluvialis fulva), and Buff-breasted Sandpipers (Tryngites subruficollis) (Alaska Interagency HPAI Bird Surveillance Working Group 2006). In addition, several populations of shorebirds intermingle with high-risk species during breeding and post-breeding (e.g., other races of Dunlin and Rock Sandpipers).
Recent technological advances allow us to follow individual migratory birds throughout their annual cycle, thus opening exciting avenues of research on the ecology and evolution of migratory birds. Using remote sensing technology, primarily satellite transmitters (PTTs) and stable isotope analyses we can connect individuals with specific sites and essentially “observe” them from afar. Bar-tailed Godwits partake of an extensive migration between Alaska and East Asia-Australasia (McCaffery and Gill 2001) and a recent satellite telemetry study discovered that the southbound leg of this migration includes the longest documented nonstop flight by a landbird (Gill et al. 2005, Gill et al., unpubl., Fig. 1).
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| Figure 1. Migration tracks of southbound Bar-tailed Godwits determined using satellite telemetry. These five individuals were tracked in 2006 as they traveled from Alaska to the southwest Pacific and New Zealand (Gill et al., unpubl.). Northbound godwits follow a route through Southeast Asia that has yet to be described in detail. |
The routes and timing of movements of northbound godwits is less clear and thus an important knowledge gap given the extensive use of stopover sites in Asia by godwits. Understanding how individual godwits use sites among multiple flyways (East-Asia Australasian, Central Pacific, Pacific) is particularly relevant based on the current distribution patterns of HPAI H5NI.
A major portion of the overall strategy for surveillance monitoring of H5N1 in North America involves sampling shorebirds in Alaska because of their direct link to Asia. We propose to continue surveillance of the high risk shorebird taxa at sites where large numbers of birds were sampled in previous years and where low pathogenic avian influenza (LPAI) was discovered in birds in 2005 and 2006 (USFWS/USGS 2007). Preliminary testing of samples from 2005 and 2006 indicated that at least seven individuals of three species (Bar-tailed Godwit, Dunlin, Rock Sandpiper) were infected with LPAI subtype(s). Although, the overall infection rate may be low, one particular group had an unusually high rate of infection; three of nine godwits (33%) sampled at Old Chevak tested positive for LPAI. The significance of this high infection rate is unclear, but warrants additional investigation given the general lack of knowledge of the ecology of AI among wild birds.
Another aspect of the ecology of AI viruses in migratory birds, namely the seasonal patterns of virus occurrence within bird populations, needs to be more fully addressed before we can understand role of migratory birds in the maintenance and spread of H5N1. H5N1 viruses are known to peak in domestic poultry in the cooler months (i.e., October-March in China; Li et al. 2004), but it is unknown if migratory birds exhibit this same pattern. By sampling within breeding populations across seasons in Alaska (i.e., spring arrival, summer breeding, fall staging) we hope to provide information that can be used to address this question.
Our field work in 2007 will address the following objectives:
- Assess the route(s), timing, and flight duration of northward migrating Bar-tailed Godwits from New Zealand
- Assess use of stopover areas in Asia by northward migrating Bar-tailed Godwits with a focus on determining proximity of godwits to current H5N1 hotspots
- For Bar-tailed Godwits from northern Alaska, determine route(s), timing, flight duration, use of Alaska stopover areas, and location of non-breeding areas
- Obtain samples in spring from shorebirds in western Alaska with a focus on recently-arrived migrants from Asia (e.g., Bar-tailed Godwits, Red Knots)
- Obtain samples in summer and fall from shorebirds in western and southwestern Alaska with a focus on recently-arrived migrants from breeding areas in Asia (e.g., Sharp-tailed Sandpipers, Rock Sandpipers) as well as post-breeding birds en route to non-breeding areas in Asia (e.g., Bar-tailed Godwits, Dunlin)
- Investigate the movement of LPAI viruses through shorebird populations in Alaska by measuring distribution of virus subtypes among species that intermix with H5N1 high-risk species at congregation sites
- Assess the efficiency of using cloacal swabs vs. oropharyngeal swabs to detect AI in shorebirds
To describe migration of northbound godwits from New Zealand, we will mark 16 birds with PTTs (8 with 25-g implantable PTTs and 8 with 10-g solar-powered PTTs attached externally). PTTs will record movements from the time of attachment (early Feb), through migration, and arrival on the breeding grounds (early May). PTTs will report every 36 h, thus providing detailed location data during the northbound flight. The solar-powered PTTs should provide information for up to two years and will allow us to map broad movements of godwits across seasons. A similar study conducted by us in 2006 determined that migratory flights of large shorebirds could be tracked successfully using satellite telemetry (Fig. 1). In addition, satellite telemetry provided information on general movement patterns of godwits and curlews (Numenius tahitiensis) at staging sites (Fig. 2).
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| Figure 2. An example of bird use of a stopover area as determined by satellite telemetry. This individual Bar-tailed Godwit spent several weeks in autumn 2006 using offshore barrier islands, coastal mudflats, and interior tundra on the southern Y-K Delta, Alaska (Gill et al., unpubl.). |
Such detailed information is not currently attainable by other methods. Work with godwits in northern Alaska will require a new effort, but will utilize personnel and equipment identified for work at other sites and knowledge gained from the similar effort in 2006.
For shorebirds in spring (May) we will collect cloacal samples (and a paired subset of oropharyngeal samples) from live birds employing methods that have worked well for us these past two years. In addition, we will collect fecal samples from individual shorebirds in situations where capture is difficult (e.g., inclement weather, trap-shy birds). Sampling sites will likely include the Tutakoke camp on the central Y-K Delta (Yukon Delta National Wildlife Refuge) and/or Wrangel Island in Russia. Both of these sites are used extensively by godwits and knots migrating between Asia/Australasia and Alaska.
For shorebirds in summer (July) we will collect cloacal samples and oropharyngeal samples from live adult godwits captured on nests or during brood-rearing. Possible sampling sites include Old Chevak camp on the central Y-K Delta, Allen Creek in the Andreafsky Wilderness, and uplands near the mouth of the Colville River on the North Slope.
For shorebirds in fall (July-September) we will continue sampling at several sites in northern and western Alaska that are utilized heavily by Asia-Alaska migrants. These sites include the coastal mudflats of the central Y-K Delta and bays on the western Alaska Peninsula. Over the past two years we have been able to collect hundreds of cloacal and fecal samples from target species at these sites.
Literature Cited
Alaska Interagency HPAI Bird Surveillance Working Group. 2006. Sampling protocol for highly pathogenic Asian H5N1 avian influenza in migratory birds in Alaska. Interagency planning report, Anchorage, Alaska.
Food and Agriculture Organization of the United Nations (FAO). 2006. Recommendations from the FAO & OIE international scientific conference on avian influenza and wild birds (Rome Italy 30–31 May 2006). http://www.fao.org/ag/againfo/subjects/en/health/diseases-cards/conference/documents/FinalRecommendations.pdf
Ducatez, M. F., C. M. Olinger, A. Owoade, S. De Landtsheer, W. Ammerlaan, H. Niesters, A. Osterhaus, R. Fouchier, and C. Muller. 2006. Avian flu: multiple introductions of H5N1 in Nigeria. Nature 442:37.
Gill, R. E., Jr., T. Piersma, G. Hufford, R. Servranckx, A. Riegen. 2005. Crossing the ultimate ecological barrier: Evidence for an 11,000-km-long nonstop flight from Alaska to New Zealand and eastern Australia by Bar-tailed Godwits. Condor 107: 1–20.
Li, K. S. and 21 co-authors. 2004. Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430: 209–213.
McCaffery, B., and R. Gill. 2001. Bar-tailed Godwit (Limosa lapponica). In The Birds of North America, No. 581 (A. Poole and F. Gill, eds.). The Birds of North America, Inc., Philadelphia, PA.
Muzaffar, S. B., R. C. Ydenberg, and I. L. Jones. 2006. Avian influenza: An ecological and evolutionary perspective for waterbird scientists. Waterbirds 29: 243–257.
USFWS/USGS. 2007. Sampling for highly pathogenic Asian H5N1 avian influenza in migratory birds in Alaska: results of 2006 field season. Progress Report, U.S. Fish and Wildlife Service (Region 7, Alaska) and U.S. Geological Survey, Alaska Science Center, Anchorage, Alaska.
Principal Investigators
Robert Gill
U.S. Geological Survey, Alaska Science Center
Anchorage, Alaska 99503
Lee Tibbitts
U.S. Geological Survey, Alaska Science Center
Anchorage, Alaska 99503
Chris Franson
U.S. Geological Survey, National Wildlife Health Center
Madison, Wisconsin 53711
Hon Ip
U.S. Geological Survey, National Wildlife Health Center
Madison, Wisconsin 53711
Cooperators
Fred Broerman
U.S. Fish and Wildlife Service, Yukon Delta National Wildlife Refuge
Bethel, Alaska 99599
Richard Lanctot
U.S. Fish and Wildlife Service, Migratory Birds Management
Anchorage, Alaska 99503
Phil Battley
University of Auckland
Auckland, New Zealand
Nils Warnock
Point Reyes Bird Observatory
Petaluma, CA 94954
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