H. Strøm1, D. Boertmann2, M. V. Gavrilo3, H. G. Gilchrist4, O. Gilg5, M. Mallory6, A. Mosbech2, and G. Yannic5,7
1Norwegian Polar Institute, Fram Centre, Tromsø, Norway
2Department of Bioscience, Arctic Research Centre, Roskilde, Denmark
3Association "Maritime Heritage: Explore & Sustain", St. Petersburg, Russia
4Environment Canada, Ottawa, ON, Canada
5Groupe de Recherche en Ecologie Arctique (GREA), Francheville, France
6Acadia University, Wolfville, NS, Canada
7Université Grenoble Alpes, CNRS, Université Savoie Mont Blanc, LECA, Laboratoire d'Écologie Alpine, Grenoble, France
- The breeding population of ivory gull in the Arctic is declining in parts of its range. Especially dramatic is the situation in Canada, where 70% of the population has been lost since the 1980s.
- Satellite tracking of ivory gulls breeding in Canada, Greenland, Svalbard and Russia show that southern Davis Strait and northern Labrador Sea is an internationally significant wintering area for the species.
- Levels of contaminants in eggs, blood and feathers of the ivory gull are among the highest ever reported in arctic seabirds and may have sub-lethal effects in combination with other stressors.
- Studies on genetics in the ivory gull show low population structure, implying that conservation planning needs to consider ivory gulls as a genetically homogeneous, Arctic-wide metapopulation.
The ivory gull (Pagophila eburnea) is a high-arctic seabird associated with sea ice throughout the year. It breeds at high latitudes, mostly in the Atlantic sector of the Arctic. Mainly small (i.e., 5 to 200 pairs), scattered colonies are found in Arctic Canada, Greenland, Svalbard and the northern islands of Russia in the Barents and Kara seas (Fig. 1). Ivory gulls breed on steep cliffs and inland nunataks (rocky outcrops emerging from icecaps), on flat, gravel-covered areas near coasts (Fig. 2) or on small islands and even gravel-covered ice floes. The species feeds on ice-associated fauna, primarily small fish and macro-zooplankton, and on remains of marine mammals killed by polar bear (Mallory et al. 2008). Migration between the high-arctic breeding grounds and the more southerly wintering areas takes place along the sea ice edge. Due to its reliance on sea ice for hunting, the ivory gull rarely moves far from sea ice. The species is listed as Near Threatened by the International Union for Conservation of Nature (IUCN), recognizing global warming and pollution as major threats (BirdLife International 2018). An international circumpolar ''Conservation Strategy and Action Plan'' has been presented by the Arctic Council to gain more insight into how this bird responds to increases in the disappearance of sea ice habitat, natural resource exploration and development and increases in contaminants (Gilchrist et al. 2008).
Fig. 1. The distribution of known ivory gull breeding colonies occupied for one or more years since year 2000 (shown here as black circles). Wintering areas are shown in light grey. Source: Circumpolar Seabird Group (CBird).
Fig. 2. Ivory gull breeding colony, Severnaya Zemlya, Russia. Photo: Alexey Lokhov.
In 2008, the Circumpolar Seabird Group (CBird) of the Arctic Council's CAFF (Conservation of Arctic Flora and Fauna) Working Group estimated the total population of ivory gulls to be 6,325-11,500 breeding pairs (Gilchrist et al. 2008). Most occur at colonies in Arctic Russia (approx. 86% of the global population). The remaining populations are more or less equally distributed between Canada, Greenland and Svalbard. The population size is difficult to assess because breeding colonies are not consistently occupied each year and because some sites may still be unknown.
The breeding population of ivory gulls is declining in at least parts of its global range. The Canadian population has declined by 70% since the 1980s at colonies that were known before 2002 (Gilchrist and Mallory 2005; Gaston et al. 2012). The reason for this decline is an area of current active research but could be related to loss of sea ice due to climate change, contaminants and illegal harvesting in Greenland during migration. The Greenland population seems to be declining in the south of its breeding range, while in the north the trends are unclear (Gilg et al. 2009). In Greenland, unusual climate events, such as very wet (rain) storms, have been shown to cause breeding failure (Yannic et al. 2014). For Svalbard, the long-term population trend is difficult to assess as historical data are scarce, but annual surveys since 2009 show a decline (Strøm 2013). Surveys conducted in the Russian Arctic in 2006-08 and incidental observations from colonies in subsequent years infer stable populations in some key colonies and no signs of an overall decline (Gavrilo and Martynova 2017). However, more recent observations in the 2010s revealed multiple events of colony abandonment or breeding failure. One possible reason is increased colony depredation by polar bears. Both the IUCN and the OSPAR-commission urge for new population surveys in all countries to better assess the status of the species and the true magnitude of decline.
Migration routes and wintering areas
While the ivory gull has long been known to winter along the southern edge of the arctic pack ice in the waters of the North Atlantic Ocean, recent results from satellite tagging of breeding birds from Canada, Greenland, Svalbard and Russia have revealed that the Davis Strait and Labrador Sea is the key wintering area for the species, at least for the Atlantic breeding populations (Spencer et al. 2014; Gilg et al. 2016) (Fig. 1). Birds from Russia (Franz Josef Land), Svalbard and Greenland aggregate in a post-breeding area along the ice-edge north of Svalbard and Franz Josef Land, and as far east as Severnaya Zemlya, before migrating along the East Greenland ice-edge to winter in Labrador and the Davis Strait (Gilg et al. 2010). Here they mix with birds from Canadian colonies (Spencer et al. 2016), making the southern Davis Strait and northern Labrador Sea an internationally significant wintering area for the species. The Bering and Okhotsk Seas also seem to be important wintering areas for the easternmost breeding population in Russia and for some Greenland and Norwegian birds, but more tracking is necessary to confirm this (Gilg et al. 2010).
As a top-predator and scavenger, the ivory gull is vulnerable to exposure to contaminants that concentrate through the food chain (biomagnifying contaminants). The levels of persistent organic pollutants (POPs) including organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs), and a heavy metal (mercury (Hg)) in ivory gulls are among the highest ever reported in arctic seabirds (Braune et al. 2006; Miljeteig et al. 2009; Lucia et al. 2015). Concentrations are not thought to be at high enough levels to cause direct mortality, but there is a threat from combined effects that are likely to have a sub-lethal effect. This has been shown in other seabird species, with similar and higher contaminant levels, with effects on parental behaviour, endocrine distribution and neurological functions, as well as to potential reproductive disruptions (Miljeteig et al. 2012; Lucia et al. 2016). The concentration of methyl mercury in feathers of Canadian birds increased by a factor of 45 during 1877-2007 (Bond et al. 2015). Mercury can have wide-ranging deleterious effects on birds. Being bioavailable, Hg levels are expected to increase in the Arctic due to global warming (Krabbenhoft and Sunderland 2013). Hence, there is concern about population effects in high-latitude species such as the ivory gull, even though such species live far from the sources of such environmental contaminants (Bond et al. 2015).
Ivory gull genetics
The ability to cope with rapid habitat changes through distribution shifts or adaptation to new conditions depends on both evolutionary and demographic processes (i.e., plasticity, adaptation or migration). The level of genetic variance within a population can directly influence the outcome of a response to environmental change by providing the necessary genetic variation upon which selection can act (Bourne et al. 2014). Until recently, the population structure of the ivory gull and the degree of connectivity between the different breeding populations was virtually unknown. Based on mitochondrial DNA-samples from museum specimens, Royston and Carr (2014) found no strong population structure, except among the birds wintering in the Pacific that probably originated from the easternmost breeding population in the Kara Sea and Severnaya Zemlya. Using a population genetic model and based on samples from 343 individuals from 16 localities across the breeding range, Yannic et al. (2016) similarly found a high degree of genetic homogeneity of ivory gulls across their entire distribution range, but with sufficient genetic diversity to maintain a genetically healthy population. The lack of population genetic structure suggests there is an effective dispersal across the Arctic region and implies that conservation planning needs to consider ivory gulls as a genetically homogeneous, Arctic-wide metapopulation (Yannic et al. 2016), with the potential to recover from other areas.
BirdLife International, 2018: Pagophila eburnea. The IUCN Red List of Threatened Species 2018: e.T22694473A132555020. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22694473A132555020.en. Downloaded on 10 September 2019.
Bond, A. L., K. A. Hobson, and B. A. Branfireun, 2015: Rapidly increasing methyl mercury in endangered ivory gull (Pagophila eburnea) feathers over a 130 year record. Proc. R. Soc. B-Biol. Sci., 282(1805), 20150032, https://doi.org/10.1098/rspb.2015.0032.
Bourne, E. C., G. Bocedi, J. M. J. Travis, R. J. Pakeman, R. W. Brooker, and K. Schiffers, 2014: Between migration load and evolutionary rescue: dispersal, adaptation and the response of spatially structured populations to environmental change. Proc. R. Soc. B-Biol. Sci., 281, 20132795.
Braune, B. M., M. L. Mallory, and H. G. Gilchrist, 2006: Elevated mercury levels in a declining population of ivory gulls in the Canadian Arctic. Mar. Pollut. Bull., 52(8), 978-982.
Gaston, A. J., M. L. Mallory, and G. H. Gilchrist, 2012: Populations and trends of Canadian Arctic seabirds. Polar Biol., 35(8), 1221-1232.
Gavrilo, M. V., and D. M. Martynova, 2017: Conservation of rare species of marine flora and fauna of the Russian Arctic National Park, included in the Red Data Book of the Russian Federation and in the IUCN Red List. Nat. Conserv. Res., 2(Suppl. 1), 10–42, https://doi.org/10.24189/ncr.2017.01 (in Russian with English summary).
Gilchrist, G., and M. L. Mallory, 2005: Declines in abundance and distribution of the ivory gull (Pagophila eburnea) in Arctic Canada. Biol. Conserv., 121, 303-309.
Gilchrist, G., H. Strøm, M. V. Gavrilo, and A. Mosbech, 2008: International Ivory Gull Conservation Strategy and Action Plan. Circumpolar Seabird Group (CBird). CAFF (Conservation of Arctic Flora and Fauna) Technical Report No. 18. 20 pp.
Gilg, O., D. Boertmann, F. Merkel, A. Aebischer, and B. Sabard, 2009: Status of the endangered ivory gull, Pagophila eburnea, in Greenland. Polar Biol., 32, 1275-1286.
Gilg, O., H. Strøm, A. Aebischer, M. Gavrilo, A. Volkov, C. Miljeteig, and B. Sabard, 2010: Post-breeding movements of northeast Atlantic ivory gull Pagophila eburnea populations. J. Avian Biol., 41, 532-542.
Gilg, O., L. Istomina, G. Heygster, H. Strøm, M. V. Gavrilo, M. L. Mallory, G. Gilchrist, A. Aebischer, B. Sabard, M. Huntemann, A. Mosbech, A., and G. Yannic, 2016: Living on the edge of a shrinking habitat: the ivory gull, Pagophila eburnea, an endangered sea-ice specialist. Biol. Lett., 12, 20160277, https://doi.org/10.1098/rsbl.2016.0277.
Krabbenhoft D. P., and E. M. Sunderland, 2013: Global change and mercury. Science, 341, 1457-1458, https://doi.org/10.1126/science.1242838.
Lucia, M., N. Verboven, H. Strøm, C. Miljeteig, M. V. Gavrilo, B. M. Braune, D. Boertmann, and G. W. Gabrielsen, 2015: Circumpolar contamination in eggs of the high-arctic ivory gull Pagophila eburnea. Environ. Toxicol. Chem., 34 (7), 1552-1561.
Lucia, M., H. Strøm, P. Bustamante, and G. W. Gabrielsen, 2016: Trace element accumulation in relation to the trophic behaviour of endangered ivory gulls (Pagophila eburnea) during their stay at a breeding site in Svalbard. Arch. Environ. Contam. Toxicol., 71(4), 518-529, https://doi.org/10.1007/s00244-016-0320-6.
Mallory M. L., I. J. Stenhouse, G. Gilchrist , G. Robertson, J. C. Haney, and S. D. Macdonald, 2008: Ivory gull (Pagophila eburnea). The Birds of North America Online, A. Poole, Ed., Cornell Lab of Ornithology, Ithaca, accessed 11 February 2014. http://bna.birds.cornell.edu/BNA/species/175/
Miljeteig, C., H. Strøm, M. G. Gavrilo, A. Volkov, B. M. Jenssen, and G. W. Gabrielsen, 2009: High levels of contaminants in ivory gull Pagophila eburnea eggs from the Russian and Norwegian Arctic. Environ. Sci. Tech., 43(14), 5521-5528.
Miljeteig, C., G. W. Gabrielsen, H. Strøm, M. V. Gavrilo, E. Lie, and B. M. Jensen, 2012: Eggshell thinning and decreased concentrations of vitamin E are associated with contaminants in eggs of ivory gulls. Sci. Total Environ., 431, 92-99.
Royston, S., and S. M. Carr, 2014: Conservation genetics of high-arctic Gull species at risk: I. Diversity in the mtDNA control region of circumpolar populations of the Endangered Ivory Gull (Pagophila eburnea). Mitochondrial DNA, 27(6), 3995-3999, https://doi.org/10.3109/19401736.2014.989520.
Spencer, N. C., H. G. Gilchrist, and M. L. Mallory, 2014: Annual movement patterns of endangered ivory gulls: The importance of sea ice. PLoS ONE, 9(12), e115231, https://doi.org/10.1371/journal.pone.0115231.
Spencer, N. C., G. H. Gilchrist, H. Strøm, K. A. Allard, and M. L. Mallory, 2016: Key winter habitat of the ivory gull Pagophila eburnea in the Canadian Arctic. Endanger. Species Res., 31, 33-45, https://doi.org/10.3354/esr00747.
Strøm, H., 2013: Birds of Svalbard. Birds and Mammals of Svalbard, K. M. Kovacs and C. Lydersen, Eds., Polarhåndbok No. 13, Norwegian Polar Institute, 86-191. https://www.npolar.no/en/species/ivory-gull/.
Yannic, G., A. Aebischer, B. Sabard, and O. Gilg, 2014: Complete breeding failures in ivory gull following unusual rainy storms in North Greenland. Polar Res., 33, 22749.
Yannic, G., J. M. Yearsley, R. Sermier, C. Dufresnes, O. Gilg, A. Aebischer, M. Gavrilo, H. Strøm, M. Mallory, R. I. G. Morrison, H. G. Gilchrist, and T. Broquet, 2016: High connectivity in a long-lived high-Arctic seabird, the ivory gull Pagophila eburnea. Polar Biol., 39(2), 221-236, https://doi.org/10.1007/s00300-015-1775-z.
December 3, 2019