Laridae: A neglected reservoir that could play a major role in avian influenza virus epidemiological dynamics

Figures & data

Figure 1. Number of studies that have focused on AIVs in Anatidae versus Laridae from 1899 to July 3, 2013. Research led on Web of Science using respectively the terms: “Influenza AND gull OR tern OR kittiwake” and “Influenza AND duck OR geese OR swan”.

Table 1. Variability in the ecology of Laridae species.

Life history traits				Implications
Population size	Abundant (e.g. herring gull; Larus argentatus)		Rare (e.g. lava gull; Leucophaeus fuliginosus)	AIV transmission more or less important
Habitat	Live in marine environments (e.g. black-legged kittiwake; Rissa tridactyla),	Live in both marine and freshwater habitats (e.g. yellow-legged gull; Larus michahellis)	Prefer freshwater habitats (e.g. ring-billed gull; Larus delawarensis)	Differential AIV transmission through abiotic reservoirs
Migration and Movements	Intercontinental migration (e.g. Arctic tern; Sterna paradisaea)	Local dispersive migration (e.g. black-tailed gull; Larus crassirostris)	Sedentary (e.g. black-bellied tern; Sterna acuticauda)	AIV transmission over longer or shorter distances and/or mostly (or not) during the breeding season
Nature of contacts with humans or domestic animal species	Direct contacts (e.g. kelp gull; Larus dominicanus).	Habitat sharing (e.g. herring gull; Larus argentatus)	Very limited contact (e.g. common tern; Sterna hirundo).	Interface between AIVs circulating in humans, domestic animals, and wildlife

Table 2. Low pathogenic avian influenza (LPAI) subtypes detected in Laridae.

	Virus
Species	Haemagglutinin	Neuraminidase	Sample type	References
Arctic tern Sterna paradisaea	H5	N3		Obenauer et al. (2006)
Black-backed gull Larus fuscus	H7, H13	N2	Serum	GenBank (2012); Hinshaw et al. (1982); NIAID (2012); Zakstel’skaja et al. (1972)
Black-headed gull Chroicocephalus ridibundus	H2, H4, H5, H6, H7, H9, H11, H13, H16	N1, N2, N3, N5, N6, N4, N8	Cloaca, trachea, feces, embryos, and tissues	Fouchier et al. (2003); Germundsson et al. (2010); Gresikova et al. (1979); Hjulsager et al. (2012); Höfle et al. (2013); Janout et al. (1979); Lewis et al. (2013); Munster et al. (2007); Spackman et al. (2009)
Black-legged kittiwake Rissa tridactyla	H4, H13, H16	N2, N3, N6	Cloaca, trachea, and serum	Hall et al. (2013); Tønnessen et al. (2011)
Black-tailed gull Larus crassirostris	H1, H2, H4, H6, H13	N1, N2, N3, N6	Cloaca, trachea, serum, feces, and tissues	Otsuki et al. (1987); Slepuskin et al. (1972); Tsubokura et al. (1981)
Common gull Larus canus	H6, H13, H16	N2, N3, N8	Cloaca and trachea	Tønnessen et al. (2013b)
Common tern Sterna hirundo	H1, H2, H4, H7	N1, N7		Becker (1966); Röhm et al. (1995)
Franklin’s gull Leucophaeus pipixcan	H6, H13	N2, N6, N9	Cloaca, trachea, and serum	Bahl & Pomeroy (1977); Hinshaw et al. (1982) (1983)
Glaucous gull Larus hyperboreus	H3, H5, H6, H13, H16	N1, N3, N8, N9	Cloaca	Ramey et al. (2010); USDA (2012)
Great black-backed gull Larus marinus	H4, H6, H11, H13, H16	N2, N6, N8, N9	Cloaca, trachea, and feces	Germundsson et al. (2010); Hjulsager et al. (2012); Munster et al. (2007); Wille et al. (2011)
Great black-headed gull Ichthyaetus ichthyaetus	H5, H9, H13	N2, N3, N6	Cloaca and trachea	L’vov et al. (2001)
American herring gull Larus smithsonianus	HA 1 to 13	NA 1 to 9	Cloaca and feces	NIAID (2012); Obenauer et al. (2006); Widjaja et al. (2004)
European herring gull Larus argentatus	H1, H2, H5, H6, H7, H10, H11, H13, H14, H16	N1, N2, N3, N4, N5, N6, N8	Cloaca, trachea, serum, and feces	Zakstel’skaja et al. (1972); Hinshaw et al. (1982); Kawaoka et al. (1988); L’vov et al. (2001); Munster et al. (2007); Germundsson et al. (2010); Marchenko et al. (2010); Kohls et al. (2011); NIAID 2012; Van Borm et al. (2012); Hjulsager et al. (2012)
Kelp gull Larus dominicanus	H13	N9	Cloaca	Pereda et al. (2008)
Laughing gull Leucophaeus atricilla	HA 1 to 13	NA 1 to 9	Cloaca and feces	Lee et al. (2001); NIAID 2012; Obenauer et al. (2006); Widjaja et al. (2004)
Mediterranean gull Ichthyaetus melanocephalus	H9	N2, N3	Trachea and feces	Lebarbenchon et al. (2009); Lewis et al. (2013)
Mew gull Larus canus	H5, H6, H13, H16	N1, N4, N6, N8	Cloaca, trachea, and serum	Germundsson et al. (2010); Kohls et al. (2011); Munster et al. (2007)
Ring-billed gull Larus delawarensis	H6, H11, H13, H16	N6	Cloaca, trachea, serum, and feces	Gaidet et al. (2010); Graves (1992); Hall et al. (2013); USDA (2012); Velarde et al. (2010)
Sabine’s gull Xema sabini	H5	N3		Obenauer et al. (2006)
Silver gull Chroicocephalus novaehollandiae	H13	N6		NIAID (2012)
Slaty-backed gull Larus schistisagus	H4	N8		NIAID (2012)
Slender-billed gull Chroicocephalus genei	H4, H9, H16	N2, N3	Cloaca, trachea, and feces	L’vov et al. (1978); Mehrabanpour et al. (2012)
Sooty tern Sterna funcata	H7, H15	N2, N6, N9	Cloaca	Mackenzie et al. (1984); Obenauer et al. (2006)
Vega gull Larus vegae	H13	N6	Cloaca and feces	Spackman et al. (2009)
Yellow-legged gull Larus michahellis	H9, H13	N2, N6	Cloaca, trachea, feces, and tissues	Lebarbenchon et al. (2007); Lewis et al. (2013); Lin et al. (2009); Van Borm et al. (2012)
Whiskered tern Chlidonias hybrida	H6	N2		NIAID (2012)

This table presents the different subtypes of LPAIVs that have been found in Laridae species by direct detection or, for serum samples, through the detection of specific antibodies.

Table 3. Highly pathogenic avian influenza (HPAI) subtypes detected in Laridae.

Species	Virus subtypes	Infection type	Host status/symptoms	Sample type	References
Black-headed gull Chroicocephalus ridibundus	H5N1	Natural and experimental	Healthy carrier, pathology, and fatal disease	Trachea and cloaca	Ellis et al. (2004); Ramis et al. (2012); Sakoda et al. (2012); Savić et al. (2010)
Brown-headed gull Chroicocephalus brunnicephalus	H5N1	Natural and experimental	Pathology and fatal disease	Trachea, cloaca, and serum	Liu et al. (2005); Ratanakorn et al. (2012)
Common gull Larus canus	H5N1	Natural	Healthy carrier		Sharshov (2010)
Common tern Sterna hirundo	H5N1 H5N3	Natural	Healthy carrier, pathology, and fatal disease	Trachea, cloaca and tissues	Becker (1966); L’vov et al. (2006)
Great black-headed gull Ichthyaetus ichthyaetus	H5N1	Natural	Pathology	Trachea and cloaca	Liu et al. (2005)
European herring gull Larus argentatus	H5N1	Experimental	Pathology and fatal disease	Trachea, cloaca, and serum	Brown et al. (2008)
Laughing gull Leucophaeus atricilla	H5N3, H5N1	Experimental	Healthy carrier, pathology, and fatal disease	Trachea, cloaca, serum, and tissues	Brown et al. (2006); Perkins & Swayne (2001)
Mongolian gull Larus mongolicus	H5N1	Natural	Fatal disease	Trachea and cloaca	Gilbert et al. (2012)
Slaty-backed gull Larus schistisagus	H5N1	Natural	Healthy carrier		Kou et al. (2009)
Slender-billed gull Chroicocephalus genei	H5N2	Natural	Healthy carrier	Cloaca	L’vov et al. (1978)

This table presents the HPAIV subtypes that have been detected in nature or studied experimentally in Laridae species by direct detection or, for serum samples, through the detection of specific antibodies.

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