January started on the same mild note on which December ended, and after a dry and bright start New Year's Day rapidly deteriorated to yet more rain and wind, with overnight temperatures of 13C (55F) in the south and damaging gales from storm “Henk”. Things improved towards the end of the first week, however, as temperatures dropped back to average across the UK, and even below average with some uncommonly cold nights, and we saw substantially more sunshine after an unusually overcast December. The cold lasted a couple of weeks before an Atlantic flow took over through the penultimate weekend, bringing more rain and some severe gales with temperatures back up into double figures for the remainder of the month. Indeed, Kinlochewe recorded 19.2C on the last Sunday, making it provisionally a new UK maximum temperature record for January and a new winter record (Dec-Feb) for Scotland.
A few tweaks have been made to a couple of the existing articles to improve clarity, and two new Chinese water deer sections looking at territoriality went live last month, one looking at territory establishment and the other at territory and home range size.
News and discoveries
Squirrelling away. Anyone who's spent time watching squirrels caching nuts will likely have noticed crows, magpies and jay following them around, often stealing the treasure as soon as the owner's back is turned. A recent study by scientists at Warsaw University of Life Sciences in Poland looked at the interactions between red squirrels (Sciurus vulgaris) and corvids (hooded crows, Corvus cornix, and rooks, C. frigileus) in a city park where the former were fed by visitors. The biologists found that despite having about every third nut pilfered and eaten by the birds, the squirrels only ever made deceptive caches when being watched by other squirrels, making no attempt to hide the location from the corvids. Contrary to what similar studies have found in greys, these reds weren't fooled by deceptive caching.
Slender shark? Many older textbooks and certain recent movies give the impression that the fearsome megalodon shark Otodus megalodon was a giant copy of the great white Carcharodon carcharias; indeed, early taxonomic studies grouped the two together as either Carcharodon megalodon or Carcharocles megalodon, until molecular data published in 2016 found that it actually belongs in the Otodus genus. The species became extinct some 3.6 million years ago and we have relatively few fossil remains to get an idea of how it looked. Previous research has suggested that it was an over-sized white shark 15 to 20 metres (50-65 ft.) long. A new review of the fossil data suggests, however, that “meg” was likely to be slimmer than modern white sharks and perhaps even longer. It is suggested that a slimmer and longer body allowed for a longer digestive tract that allowed more efficient nutrient extraction and allowing longer between meals.
Imperative otters. Many of us will have seen footage on wildlife documentaries of sea otters (Enhydra lutra) wrapping themselves in seaweed to help anchor them while they sleep. We've known for a while that kelp forests are an important habitat for these largely aquatic mammals, but a new study suggests that otters are also important for kelp forests. Monterey Bay scientists used historical surveys of kelp forests dating back to the early 1900s to estimate canopy extent, annual variation in biomass and carbon storage. The results suggest that forests declined in all regions except those where sea otters were present. The modelling showed sea otter population density was the strongest predictor of change in kelp coverage.
Seasonal highlight – Hibernation. Just a long nap?
For centuries nature-watchers noticed that certain species are either much less common or nowhere to be found during the winter months. Many early naturalists proposed explanations for these absences that, to the modern reader, may seem fanciful, if not downright bizarre. Aristotle was probably the first person to teach about hibernation, in the third century BC, and he got a surprising amount right, although he also misinterpreted quite a bit, too. He considered, for example, that redstarts moulted out of their normal plumage and became robins for the winter, before moulting back into redstarts in the spring, a phenomenon he called “transmutation”. We now know, of course, that redstarts migrate out of Greece to spend the winter further south, while robins migrate into Greece from northern Europe to overwinter. The idea that one species turns into another may seem far-fetched now, but at the time it was a way of explaining the disappearance of one species and the appearance of another without the benefit of ringing studies or satellite tracking.
Aristotle also believed that many birds spent the winter in a dormant state in trees or caves until the spring, and such theories have been rather persistent. Medieval texts talk about how the barnacle goose develops from goose barnacles attached to driftwood, while swallows were long thought to spend the winter buried in muddy riverbanks. The expansion of interest in these subjects, particularly since the 1600s, has shown us that no birds hibernate—most simply up sticks and move somewhere warmer. Leaving's not an option for everyone, though.
Opting out of the winter
Most people know that some animals from a wide range of species spend the winter “asleep”, and that this sleep is often referred to as hibernation, but what actually is hibernation? Well, the term hibernation is thought to stem from the Latin hibernare, meaning to 'spend the winter' and, although there is no universal scientific agreement the subject, it's clearly more complicated than just sleeping through the winter and waking up in the spring.
Sleep is a physiological necessity (the handful of cases where people haven't slept for more than a decade notwithstanding) because the body needs 'downtime' to repair and replace cells, consolidate memories, and grow. Hibernation, by contrast, is much more extreme and, far from being essential, can be fatal. Different species experience hibernation in different ways, but all true hibernators seem to experience a significant drop in body temperature to closely match the ambient conditions, a substantial decrease in heart rate (known as bradycardia), and a slowing of their metabolism. It is this change in physiological state that means we tend to be quite specific about the species that we think hibernate. Interestingly, for example, the species that most people would probably associate with hibernation, the brown bear, hardly reduces its body temperature and metabolism at all, implying a different physiological state: bears seem to undergo something more akin to winter lethargy than actual hibernation.
While an animal is in hibernation it relies on fat reserves to meet its much-reduced energy demands, and most of the energy used during hibernation is released by metabolising so-called white fat (white adipose tissue, WAT). When the time comes to 'wake up', invertebrates, reptiles and amphibians can rely on a rise in ambient temperature to raise their body temperatures to the point where they can resume activity. Mammalian hibernators, by contrast, do not have that luxury because mammals are what we call endotherms; they maintain their body temperature higher than the ambient by burning (metabolising) their food to produce heat. This means they must raise their body temperature 20C (68F) or more above the air temperature. To achieve this rapid warming, a special fatty tissue is employed: brown adipose tissues (brown fat, BAT).
BAT is found as lobes of orangey-brown tissue around the shoulders of hibernating mammals and is different to WAT in several ways. Most notably, BAT contains a much higher density of little organelles called mitochondria, which are essentially cellular powerhouses where energy is produced to fuel the body's cells. BAT is also riddled with capillaries and nerves. The way BAT is metabolised is fascinatingly complex, but the gist is it contains a special protein called thermogenin that allows the breakdown to produce heat rather than ATP and generates about 20 times more heat than metabolising the equivalent amount of WAT. Cold blood can then be pumped through it to warm it up before it flows to the rest of the body.
So, an animal needs to have enough WAT to supply it with energy during the hibernation and enough BAT to wake it up when spring arrives; without both, hibernation is merely a prelude to death. Why, though, should such a major physiological change be necessary? Why bother hibernating at all?
To hibernate, or not to hibernate...
To function normally, all animals need their body temperature to be within certain limits because bodies are essentially a collection of cells inside of which a vast array of chemical reactions take place. These chemical reactions are vital to our survival but are heavily influenced by temperature, and there is a general rule of thumb in chemistry (known more formally as Arrhenius' equation) that goes: for every 10C (18F) rise in temperature the rate of a chemical reaction doubles, and vice versa. So, allowing the body to cool saves energy, slowing the chemical reactions of metabolism, but at the same time means other chemical reactions, such as those that allow muscles and nerves to work, also slow down, and activity grinds to a halt. Hence, life struggles when it's too hot or cold.
Different animals keep their bodies within this so-called “Goldilocks range” in different ways. Many species manage their body temperature behaviourally. Snakes and lizards bask in the sunshine to warm up and seek shade to cool down, for example, which is known as behavioural thermoregulation. This is very effective, because using the sun's energy to warm you doesn't require burning fat, meaning that these ectotherms need much less food than comparably sized endotherms. The downside is that at some times of the year—particularly in seasonal countries—it's simply too cold to rely on solar radiation to keep you warm. By contrast, mammals metabolise food to keep warm, but this means that their food supply is crucially important—if they can't get enough, they run out of energy. Unfortunately for mammals such as hedgehogs, bats and dormice that feed primarily on ectothermic prey that can't readily be cached, such as worms, beetles, flies, moths, and molluscs, and fruit, much of their food supply disappears during the coldest months.
An additional consideration for small mammals in winter is heat loss, with small bodies (such as dormice and bats) losing heat more rapidly than larger ones, thus needing to eat proportionally more to maintain their body temperature. An eight gram (0.3 oz.) little brown bat, for example, burns through just over three times more energy per day than is needed by a 180 g (6.3 oz) false vampire bat. So, if you're a small animal and you lose heat rapidly, you must eat plenty to have sufficient fuel to keep your metabolism going and this becomes more critical the colder the weather gets. Small mammals have evolved to survive the cold, lean times of winter by adopting one of two strategies: they either cache (store) spare food that they find during the summer and autumn and rely on this larder during the winter (e.g., squirrels, wood mice, bank voles, etc.), or they feed voraciously during autumn to lay down fat and then enter into the prolonged torpor of hibernation and rely on those fat reserves. The economy of energy that hibernating mammals gain comes at the price of total immobilisation, however.
On your marks, get set, hibernate!
One of the big questions in biology is what triggers hibernation, and the answer is we don't know. In mammals, some researchers think it's instigated by one or more blood-borne substances sometimes referred to as Hibernation Inducement Triggers, or HITs, that kick in in response to environmental changes, when the nights start drawing in, temperatures drop and feeding opportunities become patchier. We still don't know much about HITs, but they seem to be opiates.
Decreasing day length seems to trigger an increase in feeding in hedgehogs (and dormice and bats), but temperature appears to be the trigger to enter hibernation, and veteran hedgehog biologist Pat Morris has demonstrated that hedgehogs can be prevented from entering hibernation if kept at 15C (59F). I should mention that while temperature's probably the most influential element, it's complex and there are no hard and fast dates for hibernation, although most hedgehogs, bats and dormice will succumb eventually, even in captivity. Some hedgehogs (typically large males) appear to start preparing as early as late August, undergoing brief periods of 'transient shallow torpor'. I'm not aware of any similar data from other mammals, but male hedgehogs tend to enter hibernation earlier than females as they're freed from the time-consuming commitments of raising a family. Among the reptiles both sexes appear to enter hibernation at about the same time.
By the time they come to hibernate, about one-third of a dormouse or hedgehog's body weight will be fat. Similarly, bats typically enter hibernation with fat reserves amounting to 20-30% of their body weight. Based on calculations of the rate at which energy is burned during hibernation, it has been estimated that hedgehogs must weigh at least 450 g (16 oz.) and dormice 12-15 g (0.4-0.5 oz) before entering hibernation, if they are to have sufficient fat reserves to survive. (It should be noted that hedgehog rescue centres, including the British Hedgehog Preservation Society, prefer to err on the side of caution and recommend a hedgehog be at least 700 g (25 oz.) before it hibernates.) The situation is not so well known for reptiles and amphibians, but it has been estimated that a newborn adder must increase its birth weight by 25%—i.e., typically put on about 1-1.5 g by eating about 12 g (0.4 oz.) of food (some 300% their birth weight!)—if it is to survive hibernation.
As the animal starts entering hibernation, several physiological changes occur in line with what we discussed at the start of this article: breathing and heartrate slows, there are some changes in blood chemistry and, ultimately, the metabolism slows as the body cools. An active hedgehog takes about 50 breaths per minute (brpm), which roughly halves while it's sleeping, and drops to 13 or fewer shallow breaths while in hibernation—this means a hedgehog takes one shallow breath every five seconds or so, compared to about two breaths per second when sleeping. Hedgehogs may even undergo brief periods of apnoea, when they stop breathing altogether; this is typically only for a minute or two at a time, but there is a dubious record of two hours between breaths! Bats in hibernation may take only a single breath every 60 to 90 minutes, reducing their oxygen consumption by about 140-times compared to their active state. The hedgehog's heart rate also drops dramatically, from around 280 beats per minute (bpm) while active (150 bpm or so while sleeping) to about 14 bpm, although this is somewhat less dramatic than that exhibited in some bats. An actively flying bat may have a heart rate of 800 bpm, which will drop to between 10-60 bpm (depending on species) during hibernation.
Hedgehogs drop their body temperature to around 10C (50F) during hibernation, while that of a dormouse falls to about 4C (39F), and some bat species go even lower, down to 2C (36F). Two Celsius is the lowest hibernating temperature recorded in a bat—typically they remain within 1-2C of the ambient. It should be noted that this is a drop in peripheral temperature (so the temperature of the skin, ears, etc.)—the core temperature (i.e., around the brain and heart) remains about normal. Various other physiological changes happen as the animal sinks into hibernation. Bats experience changes in their pancreas and some of their bones start breaking down as the marrow is replaced with fat. In hedgehogs entering hibernation, WAT metabolism drops to about 2%, carbohydrate metabolism halves, and oxygen demand to tissues drops by 98%. Magnesium also builds up in the hedgehog's blood, which is thought to help reduce blood pressure, while white blood cells are redirected to the gastrointestinal tract, presumably to help combat infection that may occur as any food in the animal's stomach starts to decompose. In mammals, the hibernation state seems to be maintained by the ratio of two hormones in the blood: when serotonin levels are high, body temperature is decreased, and when noradrenaline rises body temperature rises and arousal follows.
Hibernating mammals aren't, as many suppose, “dead to the world”. Light, being touched, and a reduction in humidity will bring bats out of hibernation at any time, although, curiously, they only appear to respond to sound at temperatures above 12C (54F). Similarly, hedgehogs will bristle to the touch and when exposed to loud noise, tucking themselves into a tighter ball. Reptiles and invertebrates do not appear to respond to most disturbances. It is also worth noting that hibernation is not a steady state. Even under laboratory conditions hedgehogs wake up periodically (it varies by individual, some arouse every 7-11 days, others may not stir for a month or more) and remain awake for a couple of days. Hedgehogs often use these periods of arousal to move nests and it is rare for a hedgehog to spend the whole winter in the same nest. Dormice also arouse periodically (arousal is twice as likely when the ambient temperature is 9C/48F as when it's 3C/37F), most often waking up during the daytime, but seldom venture out—most drop back into hibernation within a couple of hours. Bats arouse, on average, every 20 days although it may vary from a few days to several weeks, and larger bats tend to wake up more often than smaller species.
Arousal may also occur in mammals if it gets very cold—all species are prone to freezing and this is fatal for mammals. Hedgehogs, bats, and dormice will wake up if the ambient temperature drops below about 1C (34F). Many ectotherms, by contrast, are extremely tolerant to freezing, and some have glycerol in their tissues that acts as antifreeze, lowering the freezing point of their body fluids. In dry and wet conditions, common lizards can survive cooling to -3C (27F) and -2C (28F), respectively and, in a 2004 paper to the Journal of Experimental Zoology, Tann Voituron and his colleagues report that these lizards could survive even when 50% of their body tissue was ice! More interesting still was the finding that the egg-laying members of this species were less tolerant of freezing than the live-bearing members. Adders, by contrast, are less cold hardy, and succumb if more than 30% of their body tissue freezes. Similarly, sand and wall lizards can't tolerate more than 28% of their body tissues freezing, and can't tolerate even short periods below -1C (30F).
Just five more minutes, mum
A change in light levels and an increase in ambient temperature seem to be key factors in triggering the arousal from hibernation in mammals, but no single factor explains all cases and there are almost certainly several factors at play here. Whatever the trigger, arousal is highly sex biased. Working in London, Nigel Reeve found that male hedgehogs were active during March, while females were rarely seen until May. Similarly, among reptiles it's adult males that emerge first, with juveniles and females arousing a couple of weeks later. Indeed, a study of adders in Sweden between 1994 and 2001 found that males emerged two weeks earlier than females or juveniles, despite going into hibernation at the same time. In a 2007 paper, Gabor Herczeg and colleagues argue that males emerge from hibernation earlier than females because they need time to initiate spermiogenesis (i.e., sperm production) and testosterone production to be ready for the short, and highly synchronised, breeding season.
In ectotherms, it seems to be a progressive warming of the air and ground that trigger arousal. Essentially, they are paralysed by the cold and as soon as it warms up enough, they resume their activity. In mammals, however, the situation is more complicated because they must bring their body temperature up to the mid-30s Celsius (mid-90s Fahrenheit), which may be 15-20C (59-68F) warmer than the air. Arousal starts with an increase in breathing and heart rate. The BAT is activated, and blood is pumped through its capillary network, where it is warmed, before flowing around the rest of the body, slowly warming the tissues. (This is similar to the water in your central heating system passing through your boiler and then around the rest of the house, warming the radiators up.)
This warming is the slow first phase of arousal. Once the animal is warm enough for muscle function to resume, it may begin to shiver, which generates additional heat, and this is the second (faster) phase. In bats, the arousal process can take as little as 10 minutes, depending on species and ambient temperature, although it may take some an hour to become fully active. Hedgehogs, by contrast, take longer; averaging three or four hours to become fully active (although it may take anywhere between two and 12 hours). In hedgehogs, the eyes will remain closed until the body temperature reaches about 20C (68F) and it will start to move around at 28C (82F).
Once out of hibernation eating and drinking is a priority for a hedgehog, having lost between 25% and 40% of its body weight, depending on the severity of the winter. It's often considered that harsh winters are tough for hibernators, but it's actually mild ones that are the problem. Remembering Arrhenius' equation (i.e., the rate of chemical reactions double for every 10C rise in temperature), and that a hibernating animal's body temperature drops to around the ambient air temperature, we can see that in a mild winter with an air temperature of 15C (59F) the animal's metabolism is theoretically twice what it would be at 5C (41F). So, in mild winters hibernator metabolism is faster and fat reserves are burnt more quickly. Worse still are winters that are characterised by periodic mild and cold spells, because the mild spells can trigger an arousal from hibernation only for the animal to be confronted by frost, snow, or ice soon after. Arousing from hibernation uses a lot of energy and, if it occurs too often, the animal may starve to death. Unfortunately for our mammalian hibernators, climate change is producing just the kind of winters that they struggle with. Add to this that hibernators are highly vulnerable to flooding, the mild, wet, and windy winters that seem to be becoming more common in response to our warming climate do not spell good news.
Hibernaculums: des res hibernation spots
Some hibernators build special robust and weather-proof nests in which to hibernate, while others just pick a suitable pre-existing site. Whatever the decision, the structure in which an animal chooses to hibernate is called a hibernaculum. As veteran hedgehog biologist Hugh Warwick put it: “... a good hibernaculum is the basis of a good hibernation.”
In his 1996 book, Hedgehogs, Nigel Reeve describes how it takes a hedgehog between one and four days to construct a hibernaculum. The process starts by gathering a pile of dry leaves and grasses under a supporting structure, which may be bramble stems, or branches in a bonfire, into which the hedgehog climbs and starts turning around. The hedgehog uses its spines to comb the leaf pile into orderly, overlapping layers. The result is a ball of interwoven leaves, about 50 cm (20 in.) in diameter, with a single chamber accessed via a short tunnel. This may sound simple, but it is remarkably effective, and the hibernaculum will maintain the temperature of the air inside between about 1C and 5C (34-41F), even though the ambient air temperature may vary between -8C and 10C (18-50F). Lab studies have demonstrated that the hedgehog's hibernation is most effective at air temperatures of 4C (39F).
Dormice also build a hibernaculum; they create a tightly woven fibrous nest, about the size of a tennis ball. These nests are often built on the ground, in the leaf litter, although they may also situate them in tree stumps, leaf-filled coppice stools, at the base of hedges, and in human-provided nest boxes. As with hedgehogs, the nest remains at 1-4C, which is ideal for the dormouse's hibernation. Hibernating on the ground is beneficial to the dormouse because the air remains moist (which reduces the need to drink and the danger of dehydrating), but it also puts them at risk from floods, predation, and trampling.
Snakes and lizards tend to hibernate underground, although they will also take advantage of tree stumps and the root systems of fallen trees if available. A tracking study of grass snakes in Dorset during the mid-1990s found they selected steep-sided vegetation banks as hibernacula, the majority of which were in woodland or along the side of roads. Similarly, a study of adders in Sweden revealed hibernation sites characterised by stony south-facing slopes without topsoil and shading trees. Reptiles may also take advantage of man-made cuttings into rock faces and hillsides (e.g., mine shafts, tunnel cuttings, etc.) or stone walls and, in the New Forest, sites with scrubby vegetation and heather are often chosen. Some lizards, particularly sand lizards, will dig themselves a shallow tunnel in the soil in which to hibernate, while others may just overwinter in deep leaf litter. Lizards tend to hibernate in solitude, while snakes are more likely to hibernate communally. Slowworms appear to be an exception—these lizards are commonly found in communal hibernation, sometimes knotted together in balls. Interestingly, it is not uncommon to find a mixture of amphibians and reptiles hibernating together, even though some are predators of others under normal conditions.
Many frogs, toads and newts will seek out a good hibernation spot under a log, in deep leaf litter, in stone walls, or in compost heaps. Some, typically male, frogs will also hibernate underwater. Indeed, ponds make pretty good hibernation locations as the temperature in the bottom waters tends to remain stable, with less danger of predation. Frogs can tolerate short periods with the surface iced, although if there's protracted ice cover oxygen levels decline and noxious gasses (e.g., carbon dioxide and hydrogen sulphide) build up; they cannot survive if the entire pond freezes. It's uncommon for toads to hibernate underwater—their rough, warty skin is less efficient at transferring gasses than the smooth, supple skin of a frog—although it happens occasionally, and large numbers of toads have been observed sitting on the bottom of fast-flowing rivers in Sweden during the winter.
During the spring and summer months, when frogs are breeding and hunting, their oxygen demands are high—they must breathe air to meet this demand and drown if they become trapped underwater. In winter, a hibernating frog doesn't need to surface to breathe, getting all the oxygen it requires through its skin. This is because, in winter, the cold water keeps the frog's metabolism low (about 60% of active rate) and reduces oxygen demands. Additionally, cold water holds more dissolved gasses than warm water. In summer, pond surface waters may be 24C (75F) or more and can only hold about 8 mg of oxygen per litre of water. Fresh water at 4C (39F), by contrast, holds about 13 mg per litre, almost twice as much. If oxygen levels start to drop (e.g., if the pond ices over gas dissolution from the air above is reduced/prevented) a frog can reduce its metabolism further, down to about 25% the active rate by switching fuel from fat to carbohydrate, which uses much less oxygen but is less efficient so uses resources more quickly. Hence, brief periods of this “anaerobic respiration” are fine, but if it goes on for too long the frog is in trouble.
Hedgehogs, unlike dormice (which might stay in their hibernaculum for months), aren't particularly faithful to their hibernacula. In a study of nests carried out in the 1960s, Pat Morris found that only two of 167 nests were occupied through the whole winter, with 60% occupied for only two months. Hedgehogs also never re-use a hibernaculum, always building new ones each year. One 1973 study in the journal Oecologia found that a quarter of hibernacula were built in the November of the year they were to be used. Reptiles and amphibians may return to the same hibernation spots year after year.
Finally, seeing an animal we expect to hibernate out and about during the winter is generally considered ominous. We have, however, seen that all hibernating mammals will wake up if it gets very cold (to prevent freezing to death) and may also move hibernaculum if disturbed (e.g., bats) or, it appears, just because they feel like it (e.g., hedgehogs). Indeed, a study of 992 sightings and road casualty records in London, collated by the London Natural History Society between 1956 and 1964 and analysed by Pat Morris for a paper to the journal London Naturalist in July 1966, found that just over 11% were in November and December. There were 32 animals (3%) recorded during January, February, or March, which are typically the coldest months.
For a round-up of Britain's seasonal wildlife highlights for late winter, check out my Wildlife Watching - February blog.