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Camargue flamingos starved in freezing conditions in 1985 and 2012 mass mortalities

The Company of Biologists

1985 was one of the worst years in living memory for the flamingo population of the Camargue, France. Over a 15 day period in January, temperatures plummeted, the lagoons, ponds and salt pans where the birds feed froze and by the time the Arctic blast had loosened its grip, almost one third of the population was dead. 'The 1985 mass-mortality shocked a generation of conservationists,' says David Grémillet from the CEFE-CNRS, France. Alan Johnson, a conservation scientist at the Tour du Valat research center, France, who dedicated 50 years of his life to protecting the iconic animals, was at the forefront of the mission to retrieve the bodies in the hope of discovering what had killed them. Later, when 1500 birds died in another severe cold snap lasting 13 days in February 2012, Grémillet, Arnaud Béchet (Johnson's successor at Tour de Valat) and Michel Gauthier-Clerc realised that they could look at the effect of both cold snaps on the birds to try to understand how wild populations will be impacted by the increasing number of extreme climatic events that are predicted as a consequence of climate change. Together, with Anne-Sophie Deville and Sophie Labaude, they began investigating what had killed the victims of both unseasonal freezes. They publish their discovery that the flamingos starved to death when their feeding grounds froze over in The Journal of Experimental Biology at http://jeb.biologists.org.

However, when the team initiated the study, they only had Johnson's weight measurements to go on for the birds that died in 1985 and it was clear that the animals were pitifully emaciated. The birds that had died in 2012 were also very thin, but the team realised that they could get a more detailed impression of the factors that had led to the deaths of the flamingos as they had access to six carcasses.

There are three distinct phases of starvation, which occur as the animal systematically consumes its fuel reserves. Each stage can be distinguished by the ratio of lipids to proteins in the body, allowing the team to identify whether starvation was a factor in the birds' deaths. Deville, Labaude and Jean-Patrice Robin painstakingly measured the lipid and protein content of leg muscles, pectoral muscles, skin and carcass. They then compared the flamingo's lipid/protein ratio with that of starving woodchucks and mallards, and could see that the flamingos were in the later stages of starvation. 'We were surprised to see how lean (virtually fat-free) the dead flamingos were,' says Grémillet. The birds had almost certainly died of starvation.

But what role had the perishing temperatures played in the birds' demise if they had not killed the birds directly? The team decided to calculate how much energy the birds required to survive during each month from January 1980 to April 2012. Teaming up with Warren Porter, Megan Fitzpatrick and Paul Mathewson from the University of Wisconsin, Madison, USA, to use their Niche Mapper™ algorithm, the team was able to see that the birds' energy demands naturally peak each year between December and February, decrease through spring and early summer as the temperatures increase, reach a minimum around July and August and then rise again through autumn back to the winter maximum.

However, when they focused on the periods of extreme cold, they found that the cold birds'energy demands increased by 5.7-7.0%, peaking in January 1985 at 2639 kJ/day for the male birds and 2201 kJ/day for the females. The team suspects that the flamingos died because the ponds where they feed froze just as their energy demands increased further, tipping the birds over into starvation. However, they suggest that the death toll was lower in 2012 because the temperatures were not as low and returned to normal more quickly than in 1985. Grémillet is also optimistic that this knowledge can be used to help manage the unique saltpan habitats to improve the year-round condition of the flamingos and better protect them from future weather extremes.

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IF REPORTING THIS STORY, PLEASE MENTION THE JOURNAL OF EXPERIMENTAL BIOLOGY AS THE SOURCE AND, IF REPORTING ONLINE, PLEASE CARRY A LINK TO: http://jeb.biologists.org/content/217/20/3700.abstract

REFERENCE: Deville, A.-S., Labaude, S., Robin, J.-P., Béchet, A., Gauthier-Clerc, M., Porter, W., Fitzpatrick, M., Mathewson, P. and Grémillett, D. (2014). Impacts of extreme climatic events on the energetics of long-lived vertebrates: the case of the greater flamingo facing cold spells in the Camargue. J. Exp. Biol. 217, 3700-3707.

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