Climate change disrupts hibernation: female Arctic squirrels shorten it, but males do not

When the cold comes, and in Alaska it arrives soon, the Arctic suslik dig deeper into the ground until they reach the earth's icy layer, the permafrost. There, these ground squirrels spend the winter lethargic. Their hibernation strategy is one of the most extreme known: they reduce their metabolic activity by up to 1% and lower their temperature until they almost freeze. In spring, when the snow begins to retreat, they emerge from their lethargy and once again become the vault key of the terrestrial Arctic ecosystem: the main herbivore, the suslik feeds foxes, lynxes, wolves, bears and eagles in regions where food is not abundant. For nearly three decades, a group of scientists has studied two populations of these rodents. The results of their work, published in Science, show that it has taken 25 years for climate change to disrupt one of the most sophisticated survival strategies shaped by millions of years of evolution: Sulik females have advanced the end of hibernation, but not males. The consequences of such a mismatch remain to be seen.

For different reasons, such as thermal amplification caused by melting ice or greater insolation, global warming is more pronounced in Arctic areas. That's why scientists use the Arctic and the species that live in it as sentinels of climate change. One of those watchers is the Arctic suslik (Urocitellus parryii), a small animal of 40 centimeters that does not exceed 800 grams that abounds throughout the Arctic strip, from Alaska to Siberia, passing through northern Canada. For almost 30 years, American researchers in Alaska have followed the life cycle of 199 of these animals to which they placed sensors, relating their behavior to local climate change.

"Our data show that the active layer, the layer of soil above the permafrost, freezes later and later in autumn, doesn't cool as much in the middle of winter, and thaws a little earlier in spring," says U.S. Forest Service scientist and lead author of the study, Helen Chmura. The average annual temperature in the study region has risen, especially in winter, since the study began in 1993. And soil freezing, which they measured at a depth of one meter, has been delayed at a rate of four days per decade. Meanwhile, the minimum temperature of the ground, which could drop below -30º, has risen almost 5º. In addition, Chmura adds, "these changes, which amount to a reduction of about 10 days of the time the soil freezes, have occurred in just 25 years, which is a very fast pace."

Learn moreHow does the bear survive during hibernation?

How have hibernating animals reacted to so much environmental change? The sensors attached to the suslik show that they have not delayed the onset of lethargy, but they have advanced their awakening by ten days, the same period in which the freezing of the surface layer of the soil has been reduced. These rodents are among the few hibernators that use thermogenic lethargy. Temperate species, such as bears, are able to lower their body temperature to match the environmental temperature of their burrow. But in the suslik, the cold can be many degrees below zero, which would freeze their tissues. To survive, this animal is able to reactivate its metabolism necessary to generate heat and avoid freezing, doing it as many times as necessary. According to this study, they now activate this survival mechanism 37 days less than 25 years ago.

Colorado State University biologist Cory Williams has been studying the Suslik for two decades, since working at the University of Alaska Fairbanks. Senior author of this study, says in an email that the key is not so much temperature: "While this change is caused by climate warming, we do not believe that temperature is the only signal, or even the most important signal, used by these animals. As part of our long-term study, we found that, as the end of hibernation approaches, females sample conditions on the surface. If there is a large layer of snow, they will go back into hibernation, lengthening it." They only leave it when there is a sufficient surface free of snow to be able to feed. And greening in these latitudes occurs earlier and earlier.

"Males end hibernation more than a month earlier than females. They do it because it takes them several weeks to get past puberty each spring."

Cory Williams, biologist at Colorado State University, United States

The most striking thing about this work is that, although males and females start hibernation at the same time, only females have shortened it in that ten days. Williams clarifies that both genders do not wake up at the same time. "Males end hibernation more than a month earlier than females. They remain underground after ending hibernation for about another month and feed on their food reserves; They do this because it takes them several weeks to get past puberty each spring and reach sexual maturity. By ending hibernation a month before females, they can ensure that they are physiologically capable of mating as soon as they emerge."

This difference in onset explains that, for now, the advance of the end of hibernation of females is not dramatic. In fact, the researchers believe that it is being positive, since they have to resort less to thermogenic lethargy, a very expensive strategy. But if the phenomenon continues, there could be a mismatch between males and females. Williams believes that, if the trend continues, "we will have a strong selection for the early termination of hibernation by males" and trusts the plasticity of these animals to respond to the climate challenge.

Most animals that hibernate do so in latitudes where it can be very cold, but not as cold as the suslik endure. In temperate regions there is no permafrost, so they do not need a mechanism as extreme as thermogenic lethargy. However, climate change is also affecting them. A review published last year, with work on some thirty species that hibernate, showed that the impact of warming is being uneven. Except for bats, for which no changes in their hibernation patterns have been detected, most rodents are shortening it. Meanwhile, some species of ursids, such as the American black bear or the European brown bear, are delaying the onset of their autumnal lethargy.

Thomas Ruf, a researcher at the Research Institute in Wildlife Ecology at the University of Veterinary Medicine Vienna, believes that climate change will have an ambivalent impact, with winners and losers: "Different species will be affected differently, depending on their sensitivity to temperature. I think bears will be the least affected, because they are exceptional at maintaining a body temperature above 30° and do not have periodic awakenings."

The bears have shortened their lethargy

However, bears are also shortening their hibernation. The study of 70 years of data collected in 12 national and natural parks in the Soviet Union and then Russia published in 2018 shows how changes in environmental conditions are affecting brown bears across the board. "They are delaying their entry into the bear and bringing forward their exit. So they spend less time hibernating," says Sevillian biologist María del Mar Delgado, first author of this study.

Delgado works at the Joint Institute for Research in Biodiversity of the CSIC, the University of Oviedo, and the Principality of Asturias. One of his fields of study is the 370 brown bears of the Cantabrian mountain range. Here it is not the cold of Russia, so "bears do not hibernate, but they do spend months in a state of lethargy," recalls the researcher. "Especially the females, who continue to enter the oysters where they end their gestation, give birth and breed until they leave in spring," he adds. Even if they don't hibernate, their problems are the same. "By advancing the moment in which they leave, they suffer greater energy stress, the females have had less time to raise the cubs and that it is hotter, it does not guarantee that there is food," he adds. The imbalance means that both in Russia and in Spain, Delgado concludes, "they have to resort to agriculture and livestock, increasing conflicts with humans."

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