The first known avian cholera outbreak among wild birds in Alaska occurred during November 2013. Liver, intestinal, and splenic necrosis consistent with avian cholera was noted, and Pasteurella multocida serotype 1 was isolated from liver and lung or spleen in Crested Auklets (Aethia cristatella), Thick-billed Murres (Uria lomvia), Common Eider (Somateria mollissima), Northern Fulmars (Fulmarus glacialis), and gulls (Larus spp.).
Avian cholera, caused by the highly contagious bacterium Pasteurella multocida, rapidly causes death in wild birds, particularly in waterfowl (Samuel et al. 2007). The disease has been reported in >180 bird species (Samuel et al. 2007). Transmission can occur by bird-to-bird contact, aerosolized bacteria, and ingestion of bacteria in contaminated environments. Outbreaks involving wild birds occur annually in North America, and evidence suggests that the disease tends to follow the migration routes of some birds, most notably Lesser Snow Geese (Chen caerulescens caerulescens; Samuel et al. 2005b). Outbreaks are explosive and can kill thousands of birds in a short time (Samuel et al. 2007).
Saint Lawrence Island (SLI) lies in the Bering Strait region of Alaska and is home to two Alaska Native communities, Gambell (63°46′46.98″N, 171°44′27.92″W) and Savoonga (63°41′42.44″N, 170°28′44.51″W). Reliance on marine resources, including birds, for subsistence remains essential for the nutritional, cultural, and economic needs of these island communities. Over 85% of subsistence-harvested resources in the region are marine derived (Ahmasuk 2008). The island’s abundance of marine resources is due largely to the influence of the Anadyr and Alaska currents, which bring cold, nutrient-rich water from the deep to the shallow shoals of the northern Bering Sea (Piatt and Springer 2003). Mixing of these currents occurs north of SLI and facilitates prey availability for piscivores (murres), planktivores (auklets), and omnivores (fulmars; Piatt and Springer 2003). All cholera-impacted species from this event occupy coastal waters surrounding SLI, which have been designated Globally Important Bird Areas of the United States (Smith et al. 2014).
In November 2013, unusual marine bird mortality off the northern coast of SLI was reported by citizens in Gambell and Savoonga to the University of Alaska Fairbanks Marine Advisory Program and the Alaska Department of Fish and Game. Observers reported hundreds of bird carcasses washing ashore near the two villages. Clinical signs in live birds included swimming in circles with heads laying over their backs and occasionally holding wings in the air. Food safety and public health were immediate local concerns.
To document the scope of the die-off, the US Fish and Wildlife Service and the US Geological Survey Alaska Science Center (USGS-ASC) contracted with island residents to survey accessible coastline and collect specimens for diagnostics and research. Twenty-one kilometers of coastline along the north side of the island were surveyed on 23–25 November 2013, during which 912 bird carcasses were recorded. Species found were Crested Auklets (Aethia cristatella) and murres (Uria spp.), with much smaller numbers of gulls (Larus spp.), Northern Fulmars (Fulmarus glacialis), eiders (Somateria spp.), a Black-legged Kittiwake (Rissa tridactyla), and an unidentified duck (Anatidae spp.). Responders were unable to conduct beach surveys on other sections of the island due to logistics, limited daylight, and deteriorating weather; therefore, the full extent of the die-off is unknown.
Specimens submitted to USGS National Wildlife Health Center, Madison, Wisconsin, consisted of three Crested Auklets, three Northern Fulmars, three Thick-billed Murres (Uria lomvia), four gulls (Glaucous [Larus hyperboreus] or Glaucous-winged [Larus glaucescens] or hybrids; species could not be determined), and one Common Eider (Somateria mollissima). Routine aerobic bacterial isolation was performed on the indicated tissues (Table 1) by using tryptic soy agar with 5% sheep blood (BD Diagnostics, Sparks, Maryland, USA) incubated for 18–24 h at 37 C, and bacterial isolates were identified by using biochemical test (API strips, BioMérieux, Marcy l’Etiole, France). Pasteurella multocida was isolated in liver from three Crested Auklets, three Thick-billed Murres, two Northern Fulmars, one Common Eider, and one gull by using the agrose gel precipitin test (Heddleston et al. 1972) and characterized as serotype 1, the most common serotype found in wild birds (Samuel et al. 2007). The bacterium was detected in liver from one gull by next-generation sequencing. Bacterial 16S rRNA gene amplicons were prepared for Illumina sequencing and combined into one multiplexed library by using established primers and protocols (Caporaso et al. 2012) at USGS-ASC. Sequencing was performed by using two 2×150 PE cycles runs on Illumina MiSeq, each including a 15% PhiX spike. With QIIME (Caporaso et al. 2010), raw Illumina sequence data were quality filtered, joined and demultiplexed, and assigned to operational taxonomic units (OTUs; representing 97% DNA sequence similarity) picked by using the open-reference workflow (Caporaso et al. 2010). Representative OTU sequences were aligned to the GreenGenes 16S rRNA gene reference database, and taxonomy was assigned by using the RDP classifier (Cole et al. 2014). No other gross abnormalities, pathogenic bacteria, viruses, or parasites were detected in birds infected with P. multocida.
This unusual mortality event was the first confirmed report of avian cholera in wild birds in Alaska (Philo 1981). It was also unusual in its impact on species not commonly associated with avian cholera mortality. Samuel et al. (2005a) found that Greater White-fronted Geese (Anser albifrons frontalis) breeding in Alaska have antibodies to P. multocida. The closest geographic outbreaks were reported on Banks Island, Northwest Territories, Canada, and involved Lesser Snow Geese (Samuel et al. 1999). Outbreaks have been reported in Common Eiders on East Bay, Nunavut, Canada (Descamps et al. 2009). Christensen et al. (1997) reported mortality of Common Eiders at wintering areas within the sea ice in Denmark due to avian cholera in 1996. The disease was reported in Common Murre (Uria aalge) in the Baltic Sea (Samuel et al. 2007).
Changes in arctic and subarctic ecosystems due to global climate change may provide an increased opportunity for novel disease outbreaks. The discovery of avian cholera in marine bird populations in Alaska suggests that P. multocida may emerge as a significant pathogen in species previously not considered high risk. The potential impacts of avian cholera in this region are of special conservation concern for the threatened Spectacled Eider (Somateria fischeri), and the world population overwinters in these waters (Petersen et al. 1999). Although P. multocida serotype 1 is not zoonotic, investigations and response to future mortality events in this region must consider public health and food security concerns, because many marine species are used as food by local communities.
We greatly appreciate the efforts of many individuals and organizations, including P. Rookok, P. Pungowiyi, D. Pungowiyi, D. Akeya, F. Kava, M. Kiyuthlook, and T. Noongwook, Native Village of Savoonga; E. Ungott, C. Irrigoo, H. Koonooka, A. Konahok, and R. Bushu, Native Village of Gambell; M. Koonooka and G. Noongwook, Alaska Eskimo Whaling Commission; R. Gerlach, Alaska Department of Environmental Conservation; L. Castrodale, Alaska Department of Health and Social Services; P. Bente and L. Hughes, Alaska Department of Fish and Game; V. Metcalf, Eskimo Walrus Commission; B. Ahmasuk, Kawerak Subsistence Program; R. Stimmelmayr, North Slope Borough Department of Wildlife Management; E. Taylor and D. Irons, US Fish and Wildlife Service; J. Pearce, L. Zeglin, and A. Reeves, US Geological Survey, Alaska Science Center. Use of trade or product names does not imply endorsement by the US government.