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Spermophilus citellusEuropean ground squirrel

By Jason Haley and Cari Mcgregor

Geographic Range

European ground squirrels (Spermophilus citellus) are native to southeast Europe. There are two main sections of their distribution. The northwestern portion of their range includes the Czech Republic, Austria, Hungary, Slovakia, Serbia, and Romania, while the southeastern limits extend into eastern Serbia, Macedonia, northern Greece, Bulgaria, Turkish Thrace, Moldova, and Ukraine. Historically, this species was also found in Germany and Poland, but they have since become extirpated in those areas. However, in recent years the species has been reintroduced to Poland. (Ramos-Lara, et al., 2014)

Habitat

European ground squirrels spend most of their time in underground burrows, which protect them from predators. They hibernate through winter and use daily torpor (short-term hibernation) to conserve energy throughout the rest of the year. During their short active season, they are most commonly found in short-grass steppe environments. This species also lives in environments modified by humans, such as pastures, sports fields, lawns, and golf courses. European ground squirrels generally live in areas with light, well-drained soil, where they make burrows. They will use these burrows to hide from predators and as a place to hibernate for six months out of the year. European ground squirrels live at elevations 0 to 800 m above sea level. (Coroui, et al., 2008; Gedeon, et al., 2011)

  • Range elevation
    0 to 800 m
    0.00 to 2624.67 ft

Physical Description

European ground squirrels are small, with round bodies and short tails. Their size varies according to many factors including age, sex, and environmental conditions. Males have body masses of 125 to 380 g, while females range from 131 to 353 g. European ground squirrels have short legs compared to the rest of their bodies. The length of head and body for males ranges from 176 to 228 mm. The length of head and body for females ranges from 174 to 217 mm. Male tail lengths range from 31 to 90 mm, whereas female tail lengths range from 38-75 mm. European ground squirrels have a total of 22 teeth, with the following dental pattern: i 1/1, c 0/0, p 2/1, and m 3/3.

European ground squirrels have small ears that are pointed at the end. Their eyes are wide apart from one another on the upper portion of their heads. Their tails are cylindrical and do not have a determined color pattern. Their fur is smooth and yellowish on the rear. This color tends to be lighter on their ventral side. There are spots on their rear that produce a mottling effect. This species has claws and four pads on each of its paws. Juveniles at 30 days of age have an average body mass of 61.4 g and are born with hair. (Ramos-Lara, et al., 2014)

  • Sexual Dimorphism
  • sexes alike
  • Range mass
    125 to 380 g
    4.41 to 13.39 oz
  • Range length
    174 to 288 mm
    6.85 to 11.34 in
  • Average basal metabolic rate
    1.272 W
    AnAge

Reproduction

European ground squirrels monogamous throughout their breeding season, although they typically select different mates the following season. They typically breed within three weeks after emerging from hibernation. Copulation typically occurs in burrows made by females. During the mating season, male ground squirrels become increasingly aggressive. Males will also travel farther away from their burrows when searching for a mate than when searching for food. Once a female selects a mate, those mates will defend the female with aggression if necessary. (Millesi, et al., 1998; Ramos-Lara, et al., 2014)

European ground squirrels reproduce once annually, typically within three weeks after emerging from hibernation. On average, their gestation period lasts around 27 days. Litter sizes vary from 2 to 9 young, which are born with an average mass of 5.25 g. Litter sizes also vary based on how young or old pregnant females are. Older females typically give birth to larger litters than those of younger females. Weaning takes between 49 and 56 days. Sexual maturity differs between male and female ground squirrels. Females become sexually mature after one hibernation period, but males become sexually active either as yearlings or after two years of age. It is unclear whether European ground have induced or spontaneous ovulation. (Ramos-Lara, et al., 2014)

  • Breeding interval
    European ground squirrels breed once yearly.
  • Breeding season
    The European ground squirrel mates typically within three weeks after coming out of hibernation.
  • Range number of offspring
    2 to 9
  • Average number of offspring
    6
    AnAge
  • Range gestation period
    25-26 to 29 days
  • Average gestation period
    27 days
  • Range weaning age
    49 to 56 days
  • Average age at sexual or reproductive maturity (female)
    9 months
  • Average age at sexual or reproductive maturity (female)
    Sex: female
    314 days
    AnAge
  • Range age at sexual or reproductive maturity (male)
    1 to 2 years

European ground squirrels reproduce once annually, typically within three weeks after emerging from hibernation. On average, their gestation period lasts around 27 days. Litter sizes vary from 2 to 9 young, which are born with an average mass of 5.25 g. Litter sizes also vary based on how young or old pregnant females are. Older females typically give birth to larger litters than those of younger females. Weaning takes between 49 and 56 days. Sexual maturity differs between male and female ground squirrels. Females become sexually mature after one hibernation period, but males become sexually active either as yearlings or after two years of age. It is unclear whether European ground have induced or spontaneous ovulation. (Huber, et al., 2002)

  • Parental Investment
  • altricial
  • male parental care
  • female parental care
  • pre-fertilization
    • provisioning
    • protecting
      • male
  • pre-hatching/birth
    • provisioning
      • male
      • female
    • protecting
      • male
  • pre-weaning/fledging
    • provisioning
      • female
    • protecting
      • male
  • pre-independence
    • provisioning
      • male
      • female
    • protecting
      • male

Lifespan/Longevity

European ground squirrels have a maximum lifespan of approximately 6.7 years in captivity. In the wild, their average lifespan is about 2.3 years. Factors that could influence lifespans of European ground squirrels in the wild likely include predation and the destruction of natural habitats in which the species dwells. (Millesi, et al., 1999; Weigl, 2005)

  • Range lifespan
    Status: captivity
    6.7 (high) years
  • Average lifespan
    Status: wild
    2.3 years
  • Average lifespan
    Status: captivity
    6.7 years
    AnAge

Behavior

European ground squirrels are strictly diurnal mammals. Everts et al. (2004) studied the 24-hour activity cycle of this species and found that, during the day, they spend 46% of their time underground in burrows. On average, this species comes aboveground 3.9 hours after dawn and are active until about 3.2 hours before dusk. 73% of their time aboveground is spent foraging for food. Although European ground squirrels live in colonies, they are not considered social animals. Each individual occupies its own burrow and does not share with nearby members of the colony. (Everts, et al., 2004)

European ground squirrels dig burrows for many purposes; they use them to hibernate, escape from predators, and give their young a safe place to develop. European ground squirrels forage and build burrows during the spring and summer to prepare for winter hibernation. They typically enter hibernation around August. Hibernation lasts around 180 days for most European ground squirrels. Emergence occurs when temperatures average above 0°C. The earliest sightings have been reported around March 18, but the majority of European ground squirrels emerge around April 1. (Ramos-Lara, et al., 2014)

Home Range

Home ranges for this species vary among the type of environment they inhabit and whether the individual is a juvenile or an adult. In steppe environments, juveniles have a minimum home range of 71 m from their burrow. The minimum for adults is 39 m. In meadow environments, juveniles have home ranges of 40 to 136 m away from their burrow, while adults have ranges of 45 to 93m away. (Turrini, et al., 2008)

Communication and Perception

European ground squirrels communicate with other members of their species using vocalizations. There are a variety of calls with a variety of purposes. Calls can indicate threats, whether or not a threat is credible, or the severity of a threat. Eight types of calls have been reported in this species: three tonal calls (alarm, scream, and chatter) and five wideband calls (grunt, rapid grunt, snarl, chirr, and pant). Alarm calls are the loudest and most commonly used. European ground squirrels can interpret whether a call is coming from a close neighbor or if it is farther away. European ground squirrels also rely on vision, hearing, touch, and smell to perceive the world. (Ramos-Lara, et al., 2014; Schneiderova and Policht, 2011)

Food Habits

European ground squirrels commonly feed on roots, shoots, leaves, and flowers. This species has also been known to consume common voles (Microtus arvalis), house mice (Mus musculus), common shrews (Sorex araneus), European moles (Talpa europaea), young northern white-breasted hedgehogs (Erinaceus roumanicus), seedlings, grains, fruits and eggs of birds, when available. When Ramos-Lara et al. (2014) examined the stomach contents of this species, three families of plants (Poaceae, Fabaceae, and Asteraceae) constituted 33 to 100% of their plant diet. European ground squirrels store seeds, grains, and fruits in their underground burrows for later consumption. (Ramos-Lara, et al., 2014)

  • Animal Foods
  • mammals
  • eggs
  • insects
  • Plant Foods
  • leaves
  • roots and tubers
  • seeds, grains, and nuts
  • fruit
  • flowers

Predation

European ground squirrels use a tunnel-block system in their burrows to protect against predation. This system involves leaving a sand heap in a tunnel entrance, which the resident squirrel will dig through and then rebuild when entering or leaving their burrow. Some of these sand blocks are found closer to the entrance of burrows to protect against aerial predators and allow for quick escape. Known predators of European ground squirrels include large whip snakes (Coluber jugularis), common weasels (Mustela nivalis), common polecats (Mustela putorius), and steppe polecats (Mustela eversmanni). (Hut and Scharff, 1998)

Ecosystem Roles

European ground squirrels are a host to a small number of coccidian parasites. The three species that have been found in European ground squirrels are Eimeria citelli, Eimeria callospermophili, and Eimeria cynomysis. There have also been three species of nematodes: Oxyuris obvelata, Physaloptera citilli, and Trichuris leporis. Other internal parasites include dwarf tapeworms (Hymenolepis nana) and a species of Acanthocephalan (Moniliformis moniliformis). Several ectoparasites are found in European ground squirrel nests as well. These include ticks (Ixodes laguri), mites (Haemogamassus citelli and Hirstionyssus criceti), and fleas (Neopsylla setosa, Citellophilus simplex, Citellophilus orientalis, Citellophilus assimilis, and Citellophilus agyrtes). (Ramos-Lara, et al., 2014)

Commensal/Parasitic Species
  • Coccidian parasite Eimeria citelli
  • Coccidian parasite Eimeria callospermophili
  • Coccidian parasite Eimeria cynomysis
  • Nematode Oxyuris obvelata
  • Nematode Physaloptera citilli
  • Nematode Trichuris leporis
  • Dwarf tapeworm Hymenolepis nana
  • Acanthocephalan Moniliformis moniliformis
  • Tick Ixodes laguri
  • Mite Haemogamassus citelli
  • Mite Hirstionyssus criceti
  • Flea Neopsylla setosa
  • Flea Citellophilus simplex
  • Flea Citellophilus orientalis
  • Flea Citellophilus assimilis
  • Flea Citellophilus agyrtes

Economic Importance for Humans: Positive

Some Gypsy communities in eastern Europe consume European ground squirrels as a part of traditional or ceremonial meals. However, this occurs on such a small scale that it does not have any serious effect on population sizes. (Coroui, et al., 2008; Ramos-Lara, et al., 2014)

  • Positive Impacts
  • food

Economic Importance for Humans: Negative

Due to the vegetation, shrubs, and flowers that make up part of their diet, European ground squirrels could be considered a pest to humans in urban and suburban environments. They has been reported to inhabit vineyards, which could possibly cause a loss of crops if a large enough population lived in the area. The species also digs burrows under vines, in golf courses, and in other suburban environments, which could potentially create a pest problem. (Coroui, et al., 2008; Ramos-Lara, et al., 2014)

  • Negative Impacts
  • crop pest

Conservation Status

European ground squirrels are listed as vulnerable on the IUCN Red List and do not have any special status on US government lists. The main threat to this species is the degradation of their natural habitats due to agricultural development. From 1998 to 2008, population declines of over 30% were estimated in the natural range for the species. The heaviest hit populations were in Romania, the Czech Republic, Greece, Austria, and Bulgaria. In Austria, European ground squirrels are limited to occupying human-altered habitats such as golf courses, airstrips, and vineyards. In Eastern Europe some religious groups use European ground squirrels as a traditional meal. To conserve this species, populations are being reintroduced to areas where they once thrived, such as Poland and Germany. (Coroui, et al., 2008)

Contributors

Jason Haley (author), Radford University - Fall 2015, Cari Mcgregor (author), Radford University, Karen Powers (editor), Radford University, April Tingle (editor), Radford University, Zeb Pike (editor), Radford University, Jacob Vaught (editor), Radford University, Galen Burrell (editor), Special Projects.

Glossary

Palearctic

living in the northern part of the Old World. In otherwords, Europe and Asia and northern Africa.

World Map

acoustic

uses sound to communicate

agricultural

living in landscapes dominated by human agriculture.

altricial

young are born in a relatively underdeveloped state; they are unable to feed or care for themselves or locomote independently for a period of time after birth/hatching. In birds, naked and helpless after hatching.

bilateral symmetry

having body symmetry such that the animal can be divided in one plane into two mirror-image halves. Animals with bilateral symmetry have dorsal and ventral sides, as well as anterior and posterior ends. Synapomorphy of the Bilateria.

carnivore

an animal that mainly eats meat

chemical

uses smells or other chemicals to communicate

colonial

used loosely to describe any group of organisms living together or in close proximity to each other - for example nesting shorebirds that live in large colonies. More specifically refers to a group of organisms in which members act as specialized subunits (a continuous, modular society) - as in clonal organisms.

diurnal
  1. active during the day, 2. lasting for one day.
endothermic

animals that use metabolically generated heat to regulate body temperature independently of ambient temperature. Endothermy is a synapomorphy of the Mammalia, although it may have arisen in a (now extinct) synapsid ancestor; the fossil record does not distinguish these possibilities. Convergent in birds.

female parental care

parental care is carried out by females

folivore

an animal that mainly eats leaves.

food

A substance that provides both nutrients and energy to a living thing.

fossorial

Referring to a burrowing life-style or behavior, specialized for digging or burrowing.

frugivore

an animal that mainly eats fruit

granivore

an animal that mainly eats seeds

herbivore

An animal that eats mainly plants or parts of plants.

hibernation

the state that some animals enter during winter in which normal physiological processes are significantly reduced, thus lowering the animal's energy requirements. The act or condition of passing winter in a torpid or resting state, typically involving the abandonment of homoiothermy in mammals.

insectivore

An animal that eats mainly insects or spiders.

iteroparous

offspring are produced in more than one group (litters, clutches, etc.) and across multiple seasons (or other periods hospitable to reproduction). Iteroparous animals must, by definition, survive over multiple seasons (or periodic condition changes).

male parental care

parental care is carried out by males

monogamous

Having one mate at a time.

motile

having the capacity to move from one place to another.

native range

the area in which the animal is naturally found, the region in which it is endemic.

omnivore

an animal that mainly eats all kinds of things, including plants and animals

seasonal breeding

breeding is confined to a particular season

sexual

reproduction that includes combining the genetic contribution of two individuals, a male and a female

stores or caches food

places a food item in a special place to be eaten later. Also called "hoarding"

suburban

living in residential areas on the outskirts of large cities or towns.

tactile

uses touch to communicate

temperate

that region of the Earth between 23.5 degrees North and 60 degrees North (between the Tropic of Cancer and the Arctic Circle) and between 23.5 degrees South and 60 degrees South (between the Tropic of Capricorn and the Antarctic Circle).

terrestrial

Living on the ground.

tropical savanna and grassland

A terrestrial biome. Savannas are grasslands with scattered individual trees that do not form a closed canopy. Extensive savannas are found in parts of subtropical and tropical Africa and South America, and in Australia.

savanna

A grassland with scattered trees or scattered clumps of trees, a type of community intermediate between grassland and forest. See also Tropical savanna and grassland biome.

temperate grassland

A terrestrial biome found in temperate latitudes (>23.5° N or S latitude). Vegetation is made up mostly of grasses, the height and species diversity of which depend largely on the amount of moisture available. Fire and grazing are important in the long-term maintenance of grasslands.

visual

uses sight to communicate

References

Coroui, C., B. Krystufek, V. Vohralik, I. Zagorodnyuk. 2008. "Spermophilus citellus" (On-line). The IUCN Red List of Threatened Species. Accessed September 09, 2015 at http://www.iucnredlist.org/details/20472/0.

Diakou, A., E. Kapantaidakis, D. Youlatos. 2015. Endoparasites of the European ground squirrel (Spermophilus citellus) (Rodentia: Sciuridae) in central Macedonia, Greece. Journal of Natural History, 49/5-8: 359-370.

Everts, L., A. Strijkstra, R. Hut, I. Hoffmann, E. Millesi. 2004. Seasonal variation in daily activity patterns of free-ranging European ground squirrels (Spermophilus citellus). The Journal of Biological and Medical Rhythm Research, 21/1: 57-71.

Franova, S. 2015. Research of foraging and resting behaviour of European ground squirrel (Spermophilus citellus) in conditions of zoological garden as a tool for its restitution back to the wild. Ecology (Bratislava), 34/2: 176-185.

Gedeon, C., G. Boross, A. Nemeth, V. Altbacker. 2011. Release site manipulation to favour European ground squirrel Spermophilus citellus translocations: Translocation and habitat manipulation. Wildlife Biology, 17: 97-104.

Hoffmann, I., E. Millesi, K. Pieta, J. Dittami. 2003. Anthropogenic effects on the population ecology of European ground squirrels (Spermophilus citellus) at the periphery of their geographic range. Mammalian Biology, 68/4: 205-213.

Huber, S., E. Millesi, J. Dittami. 2002. Paternal effort and its relation to mating success in the European ground squirrel. Animal Behaviour, 63/1: 157-164.

Huber, S., E. Milessi, M. Walzl, J. Dittami, W. Arnold. 1999. Reproductive effort and costs of reproduction in female European ground squirrels. Oecologia, 121/1: 19-24.

Hulova, S., F. Sedlacek. 2008. Population genetic structure of the European ground squirrel in the Czech Republic. Conservation Genetics, 9/3: 615-625.

Hut, R., A. Scharff. 1998. Endoscopic observations on tunnel blocking behaviour in the European ground squirrel (Spermophilus citellus). Zeitschrift fur Sangetierkunde, 63/4: 377-380.

Koshev, Y. 2008. Distribution and status of the European ground squirrel (Spermophilus citellus) in Bulgaria. Lynx, 39/2: 251-261.

Krystufek, B., P. Glasnovic, S. Petkovski. 2012. The status of a rare phylogeographic lineage of the vulnerable European souslik Spermophilus citellus, endemic to central Macedonia. Oryx, 46/3: 442-445.

Mateju, J., P. Nova, J. Uhlikova, S. Hulova, E. Cepakova. 2008. Distribution of the European ground squirrel (Spermophilus citellus) in the Czech Republic in 2002-2008. Lynx, 39/2: 277-294.

Millesi, E., S. Huber, J. Dittami, I. Hoffmann, S. Daan. 1998. Parameters of mating effort and success in male European ground squirrels, Spermophilus citellus. Ethology, 104/4: 298-313.

Millesi, E., A. Strijkstra, I. Hoffmann, J. Dittami, S. Daan. 1999. Sex and age differences in mass, morphology, and annual cycle in European ground squirrels, Spermophilus citellus. Journal of Mammology, 80/1: 218-231.

Ramos-Lara, N., J. Koprowski, B. Krystufek, I. Hoffmann. 2014. Spermophilus citellus. Mammalian Species, 46/913: 71-87.

Schneiderova, I., R. Policht. 2011. Alarm calls of the European ground squirrel Spermophilus citellus and the Taurus ground squirrel S. taurensis encode information about caller identity. Bioacoustics: The International Journal of Animal Sound and its Recording, 20/1: 29-43.

Stewart, J., T. van Kolfschoten, A. Markova, R. Musil. 2003. Neanderthals and Modern Humans in the European Landscape During the Last Galaciation. University of Cambridge: McDonald Institute for Archaeological Research.

Turrini, T., M. Brenner, E. Millesi, I. Hoffmann. 2008. Home ranges of European ground squirrels (Spermophilus citellus) in two habitats exposed to different degrees of human impact. Lynx, 39/2: 323-332.

Weigl, R. 2005. Longevity of Mammals in Captivity; from the Living Collections of the World. Stuttgart: Kleine Senckenberg-Reihe 48.

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