Ground-Dwelling Sciurids and Hibernation
The squirrel family (Sciuridae) is among the most diverse families in the order Rodentia. In general, squirrels are thought of as living in trees, and ground-dwelling forms are often overlooked. Of over 280 species of sciurids, nearly half of them are ground dwelling. Of those, all are in the subfamily Sciurinae, which Barash (1989) divides into 3 tribes in North America: Tamiini (chipmunks), Marmotini (antelope squirrels, prairie dogs, marmots, and ground squirrels), and Sciurini (pine squirrels, other tree squirrels). However, Wang et al. (1978) places the pine squirrels (Tamiasciurus spp.) in the tribe Tamiasciurini.
Hibernation is a phenomenon that has intrigued scientists for many years (Lyman et al. 1982). When an animalís body temperature is less than the surrounding temperature, this is referred to as deep torpor or deep hibernation. Mayer (1964) states that hibernation means any state of torpor. It is most common in small mammals, especially insectivores (Mayer 1964), bats and rodents (Pough 1999). Depending on the species, ground dwelling sciurids begin to hibernate at a certain time of the year. Except for antelope squirrels, all groups of North American ground dwelling sciurids hibernate. Smaller species, especially ground squirrels living in the southwestern United States, usually estivate in the summer to escape the heat. They do not usually emerge from estivation, so they end up hibernating throughout the fall and winter (Hartson 1999), giving them perhaps the longest dormancy of any mammal.
It has been suggested that hibernation is a reversion to an ancient ectothermic trait (based on the fact that the temperature is almost the same as the surroundings, and that the animals do not need to eat much), but this theory has not been widely accepted (Lyman et al. 1982). Davis (1976) states that ancient squirrels had the ability to become torpid under unfavorable conditions on a daily basis, and this eventually led to a circadian rhythm that governs several species. Cold weather is a determining factor in the adaptation of hibernation in sciurids. The ability for circulation and respiration to slow down when the temperatures drop is a unique adaptation (Wang 1978).
One advantage of hibernation is the ability to store fat, which unlike food, is freely available and cannot be stolen (Davis 1976). There is substantial variation in the adaptation of fat storage among the groups of hibernating sciurids.
Types of Ground-dwelling Sciurids
Antelope squirrels. Antelope squirrels (Ammospermophilus spp.) are five species of relatively small (85-160 g) ground squirrels that are named for their antelope-like gait when fleeing from predators. The genus name means "lover of sand and seeds" (Hartson 1999).
The primary habitats for these squirrels are deserts in southwestern United States and northern Mexico. Antelope squirrels feed primarily on cactus fruit, yucca seeds, mesquite beans, and insects (Hartson 1999). The Nelsonís antelope squirrel (A. nelsoni) eats mostly green vegetation from December to May, and insects during the rest of the year (Murie and Michener 1984).
Reproduction in antelope squirrels involves "boxing matches" between young males competing for females, with the winner moving up in a social hierarchy (Hartson 1999). The rapidly growing young are born in early spring. The eyes of the young, depending on the species, open at the age of four or five weeks (Murie and Michener 1984).
Antelope squirrels are the only genus of ground-dwelling sciurids that do not truly hibernate. However, the white-tailed antelope squirrel (A. leucurus) may become inactive during cold weather (Hartson 1999). It may be advantageous to be small when living in the desert, because heat stress may not be as severe. This is probably why antelope squirrels do not need to estivate. Another advantage is the ability for these animals to store heat during their periods of activity because of their variable body temperatures (Pough et al. 1999).
Prairie Dogs. Prairie dogs (Cynomys spp.) are large (650-1360 g) ground squirrels found in prairies in the central United States and parts of southern Canada and northern Mexico. They are named for their dog-like call and are close cousins of ground squirrels (Hoogland 1995). In addition, the Latin name Cynomys means "dog-mouse" (Woods 1980).
The main habitats of prairie dogs are short grass prairies. The majority of their food is grasses and other herbs, but they may also eat insects and the young of non-kin prairie dogs (Hoogland 1995). During the winter when succulent grasses are scarce, black-tailed prairie dogs (C. ludovicianus) will eat prickly pear cactus as a primary food item (Murie and Michener 1984).
Prairie dogs are very social and are always found in coteries. A coterie consists of a male, several females, and their offspring. Polygyny exists in all prairie dogs species, but the intensity is varied (Murie and Michener 1984). They state that male black-tailed prairie dogs, like a few other ground-dwelling sciurid species, defend territories that include groups of females. Clark (1977) observed "kissing" among white-tailed prairie dogs. This behavior may help prairie dogs recognize kin or potential mates.
Of the five species of prairie dog, only the Gunnisonís, white-tailed, and Utah prairie dogs (C. gunnisoni, C. leucurus, and C. parvidens, respectively), undergo hibernation (Hoogland 1995). In mid-July, adult male white-tailed prairie dogs go into estivation (which later becomes hibernation), several weeks before adult females (Clark 1977). Juveniles begin to hibernate in late August. Both sexes and all age classes emerge from hibernation in March.
Marmots. Marmots (Marmota spp.) are large ground squirrels found in Europe, Asia, and North America. The hoary marmot (M. caligata), weighing 3.6-9.1 kg (8-20 lbs.), is the largest member of the squirrel family (Hartson 1999).
Marmots may live in several different habitats depending on species but avoid dense forests and wetlands (Barash 1989). Marmots are generally herbivorous, eating a variety of grasses and other plant material (Hartson 1999). Occasionally marmots may eat caterpillars, locusts, or carrion when vegetation is in low supply (Barash 1989).
Like prairie dogs, marmots live in colonies, but not quite as large. Males may have harems of at least 2 females. Nonetheless, marmots may shift from monogamy to polygamy, or vice versa, depending on the mortality and recruitment of the females. Mating takes place a few weeks after hibernation is over. Atypical of rodents, marmots do not mate until their second or third year of life. Vancouver Island marmots (Marmota vancouverensis) may not mate until their fourth summer (Woods 1980). Play fighting among male and female marmots is often observed before mounting (Barash 1989).
Marmots are the largest animals that undergo deep hibernation (Pough 1999). All marmots store body fat before they hibernate (Davis 1976). The body temperature of woodchucks (M. monax) may drop from 38ļC to as low as 8ļC (Woods 1980). Males generally emerge from hibernation 3-4 weeks before females (Murie and Michener 1984).
Ground squirrels. Ground squirrels are found in four continents of the world, representing ten genera (excluding Ammospermophilus, Marmota, and Cynomys). The genus that is focused primarily on is Spermophilus, the largest genus in the squirrel family (Sciuridae). Spermophilus has 38 species found only in the Northern Hemisphere (North America, Asia, and Europe). This genus has a wide weight range, from the 85-gram Mojave ground squirrel (S. mohavensis) to the Columbian ground squirrel which can weigh up to 820 grams. Ground squirrels are often mistakenly called "gophers," which are members of the family Geomyidae (Woods 1980).
The prime habitats of ground squirrels are dry areas. They may, however, be found in a variety of habitats such as tundra, forests, prairies, and mountains depending on the species. Ground squirrels are generally omnivorous, eating vegetation, insects, and occasionally small vertebrates (Hartson 1999). There is variation among species, of course, and the Franklinís ground squirrel (S. franklinii) probably eats the most animal material. They are known to eat duck eggs in the wild and laboratory mice in captivity (Murie and Michener 1984). The thirteen-lined ground squirrel may eat harmful insects (Woods 1980).
Typical of ground-dwelling sciurids, ground squirrels reproduce after emergence from hibernation (Michener 1985). Environmental and physiological constraints depend on the time ground squirrels end hibernation and begin to reproduce (Murie and Michener 1984). The young of some ground squirrels, such as the Arctic ground squirrel (S. parryii) may reach adult size at the year of their birth in order to begin hibernation as adults (Mayer 1964).
Most ground squirrels begin hibernation in the fall, but estivating species such as the Washington ground squirrel (S. washingtoni) start hibernating in July (Hartson 1999). The ability to store fat during hibernation is beneficial, and larger species of ground squirrel generally store more fat than smaller ones. This is particularly advantageous to ground squirrels living in northern latitudes, which are usually larger than species in southern latitudes (Fig. 1). In the expansive winter wilderness of the arctic, the only mammal that is present is the hibernating Arctic ground squirrel (S. parryi) (Mayer 1964).
Chipmunks. Chipmunks (Tamias spp.) inhabit North America and northern Asia, with 24 species in the former continent and a single species (T. sibiricus) in the latter. They are the smallest ground dwelling sciurids, weighing from 28 grams for the alpine and least chipmunks (T. alpinus and T. minimus, respectively) to up to 142 grams for the eastern chipmunk (T. striatus) (Hartson 1999). Not long ago the eastern chipmunk was considered to be the sole member of the genus Tamias and all the other chipmunks were placed in Eutamias.
Habitats of chipmunks are variable depending on the species. Several types of habitats are preferred, such as rocky slopes, deserts, and woodlands. Diet is also variable among different species of chipmunk. Fungi, seeds, insects, and nuts are among the favorite foods of most chipmunks. Much of the food is stored in cheek pouches and hoarded in their burrows for the winter (Hartson 1999).
Unlike most other ground-dwelling sciurids, chipmunks show reversed sexual dimorphism. In most species, the female is larger than the male. Another oddity, in relation to similar genera, is that chipmunk reproduction involves a courtship ritual. Like tree squirrels, males often follow and fight over estrous females. This is termed nondefense polygyny because males do not successfully defend the female or the area she has occupied (Murie and Michener 1984). After mating, the male and the female will stay together for an hour or two for a "honeymoon" before the female chases the male away (Wishner 1982). Although sciurids generally avoid extreme inbreeding (Barash 1989, Hoogland 1995), there is a documented case of a female eastern chipmunk producing a litter sired by her 7-month-old son (Wishner 1982).
Even though chipmunks enter hibernation, they are not typical deep hibernators (Lyman et al. 1982). They can be torpid for a few days alternating with a day of activity (Wishner 1982). This may be because it is energetically inexpensive for such small animals to arouse from torpor frequently (Pough 1999). Before hibernation, most western chipmunk species store fat, and the eastern chipmunk (T. striatus) does not. Evidently, chipmunks are too small to use their fat storage as a hibernation strategy, but weight gain can be measured (Davis 1976). Most species will undergo a semitorpid state. Chipmunks tend to hibernate longer and more often in higher latitudes than in lower ones. The gray-collared chipmunk (T. cinereicollis) of southern Arizona and New Mexico may not hibernate at all (Hartson 1999).
Adaptation of Hibernation
When food is scarce and temperatures are extreme, many species have adapted by hibernating. Murie and Michener (1984) state that hibernation may be a factor in the water balance. According to Barash (1989), hibernation is influenced by food deprivation and simplified by body shape, prominently the presence of an abundance of fat. Other factors influencing the onset of hibernation may include food availability, light, fat storage, food storage, and environmental temperature (Mayer 1964). Such factors affect the endocrine glands, which act upon the hibernator via hormones. Because squirrels are mammals, they are bound up with the occurrence of endothermy and the control of body temperature (Lyman et al. 1982).
Hibernation is not necessarily the same as torpor. Hibernation refers to the long period of time animals remain torpid in their burrows during the winter, and torpor is a state of lowered body temperature that lasts as short as a few hours (Davis 1976). Estivation is a term used to describe escape from the summer heat. Wangís (1978) study on Richardson ground squirrels (S. richardsonii) shows that there are several periods of torpidity during hibernation, and the animals frequently arouse from torpor without emerging from hibernation. Duration of torpor is generally longer in the winter than in the fall.
Marmots, on the other hand, most likely do not repeatedly arouse from torpor due to the fact they are deep hibernators. It is also energetically and reproductively more efficient for them to remain hibernating than to arouse too early (Barash 1989).
Ground-dwelling sciurids typically hibernate in an underground chamber known as a hibernaculum. Male Richardson ground squirrels store food in this underground chamber as the primary source of energy during hibernation (Michener 1993). This may be why they arouse from torpor frequently. Despite the social nature of ground squirrels and marmots, they do not share hibernacula (Barash 1989 and Michener 1993). Mayer (1964) states the sharing of sleeping chambers may pose a risk of cannibalism. Additionally, monogamous hoary marmots (M. caligata) in Alaska may need hibernacula 500 meters apart from one another, which is too great a distance for a male to defend more than one (Barash 1989).
In most hibernating sciurids, including ground squirrels, chipmunks, marmots and prairie dogs, males emerge from hibernation before females (Clark 1977, Woods 1980, Murie and Michener 1984, and Barash 1989). There are several possible reasons for this behavior. Barash (1989) states that adult male woodchucks (M. monax) must compete for females before the females emerge. In the Richardson ground squirrel (S. richardsonii), early emergence may improve reproductive success of the male (Murie and Michener 1984). On the other hand, Murie and Michener (1984) state that juvenile males emerge after juvenile females in most Spermophilus species. This is probably because the young females are reproductively mature before the males.
There are also sex and age differences in the scheduling of immergence into hibernation. In general, adult males immerge into hibernation first, then adult females, then subadults, and then juveniles. However, in Arctic, Uinta, and Wyoming ground squirrels (Spermophilus parryi, S. armatus, and S. elegans, respectively), females go into hibernation before males (Murie and Michener 1984). There also is a difference in immergence time between maternal females and non-maternal females, with the latter entering hibernation first (Murie and Michener 1984 and Barash 1989).
Depending on latitude, ground squirrels, even within the same species, emerge from hibernation at different times (Davis 1976). The little suslik (S. pygmaeus), a small ground squirrel inhabiting the former Soviet Union, emerges from hibernation during early March in the southern part of their range and late March farther north (Ognev 1963). Southern species, such as the round-tailed ground squirrel (S. tereticaudatus) emerge between January and March, whereas northern species, such as the Arctic ground squirrel (S. parryi) emerge from April to May (Murie and Michener 1984). Marmots have both interspecific and intraspecific variation in timing of hibernation onset, and high-latitude populations show decreased seasonal variation in their yearly cycles (Barash 1988). Figure 2, based on a table from Murie and Michener (1984), shows the relationship between three latitudes and emergence from hibernation in the woodchuck (M. monax).
Hibernating intensity is strongly correlated with body size. Lyman et al. (1982), however, states that the length of a hibernation bout in mammals is not correlated with size. This may be because several different types of mammals were used in their study, and sciurids may be unique. Of the Marmotini, species shorter than 200 mm hibernate irregularly or not at all, and species longer than 200 mm are concordant hibernators and estivators (Davis 1976). In marmots, size may be an important factor in hibernation success because these large rodents can store more fat, diffusing it more slowly (Barash 1989). Understandably, sciurids tend to be heavier at higher latitudes (following Bergmanís rule), and would therefore be better adapted to hibernation in areas experiencing harsher winters. Figure 3 shows that species of Marmota show their species abundance peak at the highest latitude, followed by Spermophilus, and then Tamias.
Many biologists are intrigued by the phenomenon of hibernation. It is important to understand the relationship between all types of ground-dwelling sciurids and their biology in order to determine how each adapts to temperature extremes by entering hibernation. Closely related hibernators, the tribe Marmotini, have been the choice for Davisís (1976) work when studying the evolution and adaptive value of hibernation. Those that do not hibernate, such as the antelope squirrels (Ammospermophilus spp.) and some prairie dogs (Cynomys ludovicianus and C. mexicanus), may have specialized ways to resist extreme temperatures other than hibernation. Such groups may give insight for comparison with hibernating sciurids, which have adapted in different ways according to their habitats, food abundance, reproduction, and other factors.
The squirrel family is among the most diverse families of mammals, exhibiting a variety of shapes and sizes, as well as a diversity of life histories and adaptations to weather extremes. Hibernation is an adaptation that is unique among certain vertebrates, especially warm-blooded animals (endotherms). As was discussed, there is considerable variation on how different ground-dwelling sciurids become accustomed to hibernation. Because of the complexity of this rare phenomenon, additional research on the adaptation of hibernation is a necessity (Mayer 1964).
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Photo credits (in order)
White-tailed Antelope Squirrel (Ammospermophilus leucurus): Charles Ott
White-tailed Prairie Dog (Cynomys leucurus): Steven Holt
Yellow-bellied Marmot (Marmota flaviventris): Tom Bean
Townsendís Ground squirrel (Spermophilus townsendii): Herbert Clarke
Colorado Chipmunk (Tamias quadrivittatus): Charles Milton
Fig. 1: Median weight of each ground squirrel (Spermophilus) species versus median latitude of their distribution. Each square represents one species.
Fig. 2. A comparison between 3 latitudes for the dates of earliest and latest hibernation emergence of the woodchuck, Marmota monax.
Fig. 3. The relationship between latitude and species density among three genera of ground-dwelling sciurids. Note: some species such as the Olympic marmot do not occur on any of the latitudes on the x-axis, so they are marked as occurring on the nearest multiple of 5 latitude. Since not much is known about chipmunks in Mexico, the number 3 for Tamias species on latitude 25 is an estimate.