SAMPLING BLACK BRANT FOR HIGHLY PATHOGENIC AVIAN INFLUENZA (H5N1) AND NON-H5N1 VIRUSES DURING NESTING, BROOD REARING, AND MOLTING

Secondary research: Variation in gosling growth and survival among breeding colonies on the Yukon-Kuskokwim Delta and in body condition of molting birds between sub-arctic and arctic coastal plain (Teshekpuk Lake area) sites in Alaska.

Justification and Background:

Avian Influenza Sampling.-Our present understanding of virus transmission within avian populations is very limited and the presence of viruses such as H5N1 may be difficult to detect.  Thus, when the Alaska Avian Influenza Working Group was tasked with establishing a sampling plan to detect H5N1 in Alaska, many questions regarding sampling strategies were raised.  For example, previous research on avian viruses found that the prevalence of a virus may vary greatly among spatially segregated segments of a population (Hollmén et al. 2003).  However, when birds are clustered in space, how many clusters should be sampled?  When is the best time to sample, soon after arrival in the spring, or later in the summer?  When birds segregate between breeding and non-breeding flocks, should we sample both?  When non-breeding flocks occur in widely ranging geographic areas, do all areas need to be sampled?  Should birds be targeted during periods of physiological stress?  Finally, juveniles are generally considered to be immune-naïve and may be sensitive indicators of the presence of viruses in a population; can sampling targeted at young birds increase the probability of detection?  Given that other avian influenza viruses are commonly found in waterfowl, a detailed comparison of non-H5N1 viruses found in populations sampled across a range of sites, breeding classifications, and ages can yield data useful for optimizing future sampling programs focused on detecting a specific virus. 

Black Brant (Branta bernicla nigricans; hereafter brant) represent one of the more extreme species of waterfowl in Alaska with regard to clustering and range of distribution.  As such, brant represent a useful species for detailed comparisons of variation in the presence of a virus within a population through space and time.  First, brant may actually contact and carry the H5N1 virus to Alaska.  Brant ranked in mid-range among 11 candidate waterfowl species for highly pathogenic avian influenza (AI) sampling (12.0; Alaska Interagency HPAI Bird Surveillance Working Group 2006).  Brant biology and movements suggest several potential pathways for transmission of AI to North America.  The eastern portion of the Russian breeding population winters in North America.  The western portion of the Russian population winters in Japan, Korea, and northeastern China, near recent outbreaks of the H5N1 virus (e.g., Hong Kong).  Mixing of flocks likely occurs between these two Russian breeding populations, and potentially with birds wintering in northern Europe.  Brant marked in Alaska have also been observed staging and wintering in Japan (Derksen et al. 1996), indicating that there is interchange between birds from Alaska and those that winter closest to infected areas.  In addition, molt migrants from Russia may come to the arctic coast of Alaska (King and Hodges 1979) and conversely molting birds from Alaska may migrate to Russia (e.g., Wrangel Island; Ward et al. 1993).  
 
Second, brant breed in a highly clustered distribution across 2 broad geographic areas in Alaska.  The primary breeding ground is the Yukon-Kuskokwim Delta (Y-K Delta); there birds nest in 4 main colonies ranging in size from 1,000−5,000 pairs.  Within each of these colonies birds tend to nest at very high densities and intra-specific competition for nest sites is high.  Thus, bird-to-bird contact is common as they fight for, and defend nesting territories.  Further, brant feed on short sedges and grasses that are maintained in grazing lawns through positive forage feedbacks (Person et al. 2003) and there is a high level of fecal contamination of forage within these grazing systems.  These behaviors create optimal conditions for spread of influenza viruses within colony units.  Conversely, across the Arctic Coastal Plain (ACP) brant nest in very small, dispersed colonies which range in size from a few to several hundred birds. 
 
Third, molting brant segregate into discrete flocks during the flightless period.  Molt flocks are made up of both non-breeders (sub-adults and some fraction of adults that skip reproduction) and failed breeders (adults that attempt reproduction, but fail).  While some molting flocks occur on the nesting grounds where birds are segregated from breeding flocks, most molting brant migrate to specific areas such as Teshekpuk Lake on the ACP where they molt in large flocks on a series of segregated lakes. Molt may also be a period of high stress for birds because they need to meet nutritional demands not only for maintenance, but also for energy/nutrient costs of feather replacement, and to regain lipid reserves for migration.

Finally, after hatch, broods disperse from nesting colonies to rear young.  Broods from various colonies are segregated across a much larger brood rearing area than the original nesting colony, but broods from separate colonies rarely mix.  Brood flocks range in size from a few hundred to a few thousand individuals.  During brood rearing, brant forage on grazing lawns where fecal contamination is high. 

Secondary Research

Variation in gosling survival and growth among breeding colonies on the Yukon-Kuskokwim Delta.-Spatial variation in gosling growth has been related to variation in forage quality (Leafloor et al. 1998) and future survival and fecundity are strongly tied to gosling growth (Owen and Black 1989, Sedinger et al. 1995). Thus, forage quality and availability can strongly influence population dynamics (Sedinger et al. 1995, Schmutz and Laing 2002).  As goose density increases, grazing by geese may reduce forage to levels where food becomes limiting and gosling growth negatively impacted (Sedinger et al. 1998, Schmutz and Laing 2002).  Thus, gosling growth should reflect the population trajectory and proximity to reaching carrying capacity (i.e., as the population approaches carrying capacity, gosling growth rates should decline and rates of population increase should flatten and then decline; Sedinger at al. 1998).  On the Y-K Delta, population dynamics differs among the different colonies (Sedinger et al. 1998).  Further, while much work has been done at the Tutakoke colony (Sedinger et al. 1995, Sedinger et al. 1998, Sedinger et al. 2001), gosling growth has not been examined for any of the other Y-K Delta colonies.  Estimates of gosling growth from other colonies will allow us to indirectly examine forage capacity for these colonies and may help explain differences in population dynamics among colonies.

Our objective would be to compare gosling growth among colonies on the Y-K Delta.  We will also estimate gosling survival and identify brood rearing areas for the Kigigak Island and Baird Inlet colonies.

Variation in the condition of the molting brant between sub-arctic and arctic sites .- The most important molting area for Black Brant is the Teshekpuk Lake area on the ACP.  Molting flocks have also been observed on the Y-K Delta, however, little is known about these brant.  Comparison of molt ecology between the ACP and Y-K delta should add to our understanding of mass loss during molt and help answer the question of why some brant choose to make the long distance migration form the Y-K Delta to the Teshekpuk lake area, a distance of >2,000 km, while others remain.
    

Methodology:

Avian Influenza Sampling

Nesting - Spring sampling will be spread across two broadly defined breeding areas: the Y-K Delta and the ACP¹.  Within each of these areas brant typically nest in colonies which we will sample as clusters.  Thus, on the Y-K Delta where colony sizes are large, we will sample 70 females from each of the 3 major colonies: Kigigak Island, Baird Inlet, and Tutakoke River².  Conversely, on the ACP, nesting colony sizes are small and samples of 10 females will be taken from 4 distinct colonies.  Females will be captured on nests during incubation using nest traps and AI samples will be taken as cloacal swabs.

Molting - In the vicinity of Teshekpuk Lake (ACP)¹ large flocks of molting brant are regularly found dispersed across a series of large lakes. We will sample lakes as clusters, 50 birds per lake from each of 4 lakes, live capturing birds in corral traps and taking cloacal swabs. On the Y-K Delta we will conduct recognizance flights to locate molting flocks of brant. After flock location, we will sample from various flocks (40-60 birds per flock, 200 birds total) to replicate the design used at Teshekpuk Lake if the distribution of birds allows.

Brood-Rearing - On the Y-K Delta², to locate broods and brood flocks after they leave the nesting colony, nesting females (30 at both Kigigak and Baird Inlet) will be trapped just before hatch and radio-marked using conventional transmitters. At Tutakoke River brood rearing areas are known. Goslings from each of these three colonies will be captured by driving brood flocks into corral traps and two hundred will be sampled by cloacal swab.

Swab samples will be sent to the USGS, National Wildlife Health Center, Madison, Wisconsin, where they will be screened by PCR for avian influenza viruses and virus isolates will be obtained from samples by inoculation of embryonated chicken eggs by the method of Senne (1998).  The H and N antigen sub-typing of the influenza isolates will use traditional serological methods and adaptation of newer molecular approaches.  Serological tests involve the use of reference sera containing mono-specific antibodies against the 15 H and 9 N antigens of avian influenza viruses.  Genome sequencing will be used to compare isolates by phylogenetic analysis to identify genetic relatedness of viruses among and within the various sub-populations of brant.

Variation in Gosling Survival and Growth Among breeding Colonies on the Y-K Delta²: Goslings will be web-tagged in the nest at hatch (1000+ web-tags per colony).  To examine total brood loss and gosling survival we will relocate brood females at approximately 30 days post hatch using aerial telemetry and we will count goslings in broods from the air.  We will capture brood flocks as described above, and we will weigh and measure web-tagged goslings (i.e., known age and colony of origin) to estimate growth rates (50 of each sex, from each colony). 

condition of molting brant at sub-arctic and arctic sites¹: We will capture molting flocks as described above, and we will weigh and measure birds, including 1st primary as indicator of molt stage, and check for brood patches on females.   

¹ Work on the ACP will be conducted as part of the DOI on the Landscape initiative conducted by scientists from the USGS, Alaska Science Center.

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.

Derksen, D.V., K. S. Bollinger, D. H. Ward, J. S. Sedinger, and Y. Miyabayashi 1996.  Black brant from Alaska staging and wintering in Japan.  Condor 98:653-657.

Flint,P.L., J.S. Sedinger, and K.H. Pollock. 1995. Survival of juvenile black brant during brood rearing. Journal of Wildlife Management 59:455-463.

Hollmén T. E., J. C. Franson, P. L. Flint, J. B. Grand, R. B. Lanctot, D. E. Docherty, and H. M. Wilson.  2003. An adenovirus linked to mortality and disease in long-tailed ducks (Clangula hyemalis) in Alaska.  Avian Diseases 47:1434-1440.

King, J. G. and J. I. Hodges. 1979. A preliminary analysis of goose banding on Alaska’s arctic slope.  Pages 176-188 in R.L. Jarvis and J. C. Bartonek (eds). Management and Biology of Pacific Flyway Geese. Oregon State University Bookstores, Corvallis.

Leafloor, J. C., D. Ankney, and D. H. Rusch. 1998.  Environmental effects on the body size of Canada geese. Auk 115:26-33.

Owen, M. and J. M. Black. 1989.  Factors affecting the survival of Barnicle Geese on migration from the breeding grounds. Journal of Animal Ecology 58:603-617.

Person, B. T., M. P. Herzog, R. W. Ruess, J. S. Sedinger, R. M. Anthony, and C. A. Babcock.  2003.  Feedback dynamics of grazing lawns: Coupling vegetation change with animal growth. Oecologia 135:583-592.

Schmutz, J.A. and K.K. Laing. 2002.  Variation in foraging behavior and body mass in broods of Emperor Geese (Chen canagica): evidence for interspecific density dependence. Auk 119:996-1009.        

Sedinger, J. S., M. S. Lindberg, B. T. Person, M. W. Eichholtz, M. P. Herzog, and P. L. Flint.  1998. Density-dependent effects on growth, body size, and clutch size in Black Brant.  Auk 115:613-620.

Sedinger, J. S., P. L. Flint, and M. S. Lindberg. 1995. Environmental influence on life-history traits: Growth, survival, and fecundity in Black Brant (Branta bernicla).  Ecology 76:2404-2414.

Sedinger, J.S., M.P. Herzog, B.T. Person, M.T. Kirk, T. Obritchkewitch, P.P. Martin, and A.A. Stickney. 2001. Large-scale variation in growth of black brant goslings related to food availability. Auk 118:1088-1095.

Senne, D. 1998. Virus propagation in embryonated eggs. In: A Laboratory Manual for the Isolation and Identification of Avian Pathogens. D. E. Swayne, J. R. Glisson, M. W. Jackwood, J. E. Pearson, and W. M. Reed (Eds), Fourth Ed. The American Association of Avian Pathologists, U. of  Pennsylvania, Kennett Square, PA. pp. 235-240.

Ward, D. H., D. V. Derksen, S. P. Kharitonov. M. Stishov, and V. Baranyuk. 1993. Status of Pacific black brant Branta bernicla on Wrangel Island, Russian Federation. Wildfowl 44:39-48.

Cooperators and Partner Projects :

USGS (Alaska Science Center) - DOI in the Landscape Initiative         
USFWS (Yukon Delta NWR)
University of Nevada, Reno

Principal Investigators:

Tom Fondell and Paul Flint
U.S. Geological Survey, Alaska Science Center
1011 E. Tudor Road, Anchorage, Alaska 99503

Chris Franson
U.S. Geological Survey, National Wildlife Health Center
6006 Schroeder Road, Madison, WI 53711