Callosciurus erythraeus (Pallas's squirrel)

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Adult

Callosciurus erythraeus; Pallas's squirrel or Red-bellied squirrel, an adult.

Noriko Tamura-Hayashi

Identity

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Preferred Scientific Name

Callosciurus erythraeus (Pallas, 1779)

Preferred Common Name

Pallas's squirrel

Local Common Names

China: belly-banded squirrel; red-bellied tree squirrel
Japan: formosan squirrel; red-bellied tree squirrel
Malaysia: mountain red-bellied squirrel
Taiwan: belly-banded squirrel; formosan squirrel; red-bellied tree squirrel
Thailand: belly-banded squirrel

Summary of Invasiveness

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C. erythraeus is a serious pest for agroforestry both in its original and its introduced range (Kuo, 1985; Torii, 1993). Population growth is rapid in introduced habitats without effective predators. This species was designated as an invasive alien species in Japan in 2005.

Taxonomic Tree

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Domain: Eukaryota
Kingdom: Metazoa
Phylum: Chordata
Subphylum: Vertebrata
Class: Mammalia
Order: Rodentia
Family: Sciuridae
Genus: Callosciurus
Species: Callosciurus erythraeus

Notes on Taxonomy and Nomenclature

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Geographical variation in colour forms is considerable. C. erythraeus includes four subspecies groups: C. erythraeuserythraeus, C. erythraeus flavimanus, C. erythraeussladeni, C. erythraeusstyani, and insular forms of Taiwan and Hainan (Corbet and Hill, 1992). The species C. flavimanus and C. sladeni, identified by Moore and Tate (1965), are included in C. erythraeus (Corbet and Hill, 1992).

Description

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Head and body length: 200-260 mm. Tail length: 170-200 mm. Ear length: 19-24 mm. Hind foot length: 45-54 mm (Abe, 2005). Body weight: 309-435 g for adult males (Tamura and Terauchi, 1994). Geographical variation is considerable with different colour forms. The dorsum is usually olive-brown agouti. The venter colour varies from entirely agouti to maroon with a central agouti stripe, or without stripe in Taiwan and the introduced populations in Japan (Corbet and Hill, 1992).

Distribution

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C. erythraeus occurs naturally in north-eastern India, Myanmar, Thailand, peninsular Malaysia, Indochina, southern China and Taiwan (Wilson and Reeder, 1992).

In Japan, introduced populations are naturalized in Izu-Oshima Island (Tokyo), the southeastern part of Kanagawa Prefecture, the western Izu Peninsula, Hamamatsu City (Shizuoka), Kinkazan (Gifu), Osaka-jo Park (Osaka), Himeyama Park (Hyogo), Tomogashima Island, Wakayama-jo Park (Wakayama), Fukue and Iki Islands (Nagasaki), and Takashima Island (Oita) (Tamura, 2002).

In Cap d’Antibes, France, and in Villa Flandria, Argentina, introduced squirrels were naturalized in the 1970s (Jouanin, 1986; Novillo and Ojeda, 2008). They were also naturalized in the Netherlands in 1998 (Dijkstra et al., 2009) and in Belgium in the 2000s (Stuyck et al., 2009).

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Continent/Country/Region	Distribution	Origin	First Reported	Invasive	Reference	Notes
Asia
Bangladesh	Present	Native			IUCN, 2009
Bhutan	Present	Native			Corbet and Hill, 1992
Cambodia	Present	Native			Corbet and Hill, 1992
China	Present					Present based on regional distribution.
-Anhui	Present	Native			Zhang, 1997
-Fujian	Present	Native			Zhang, 1997
-Guangdong	Present	Native			Zhang, 1997
-Guangxi	Present	Native			Zhang, 1997
-Guizhou	Present	Native			Zhang, 1997
-Hainan	Present	Native			Zhang, 1997
-Henan	Present	Native			Zhang, 1997
-Hubei	Present	Native			Zhang, 1997
-Hunan	Present	Native			Zhang, 1997
-Jiangsu	Present	Native			Zhang, 1997
-Jiangxi	Present	Native			Zhang, 1997
-Shaanxi	Present	Native			Zhang, 1997
-Shanghai	Present	Native			Zhang, 1997
-Sichuan	Present	Native			Zhang, 1997
-Tibet	Present	Native			Zhang, 1997
-Yunnan	Present	Native			Zhang, 1997
-Zhejiang	Present	Native			Zhang, 1997
India	Present					Present based on regional distribution.
-Assam	Present	Native			Corbet and Hill, 1992
-Sikkim	Present	Native			Corbet and Hill, 1992
Japan	Present					Present based on regional distribution.
-Honshu	Localised	Introduced	1930s	Invasive	Tamura, 2002	First introduction in 1930s. Found on two small islands and in seven localities on Honshu
-Kyushu	Localised	Introduced		Invasive	Tamura, 2002	Found on three small islands and in one locaility on Kyushu
Laos	Present	Native			Corbet and Hill, 1992
Malaysia	Present					Present based on regional distribution.
-Peninsular Malaysia	Present	Native			Corbet and Hill, 1992
Myanmar	Present	Native			Corbet and Hill, 1992
Taiwan	Present	Native			Zhang, 1997
Thailand	Present	Native			Corbet and Hill, 1992
Vietnam	Present	Native			IUCN, 2009
South America
Argentina	Localised	Introduced	1973	Invasive	Novillo and Ojeda, 2008	Individuals reared on a ranch escaped and established in Villa Flandria, Buenos Aires
Europe
Belgium	Localised	Introduced	2000s	Invasive	Stuyck et al., 2009	Introduced to the 'Dadipark' amusement park in the town of Dadizele.
France	Localised	Introduced	1970s	Invasive	Gerriet, 2009	Introduced to Cap d'Antibes (Alpes-Maritimes)
Netherlands	Localised	Introduced	1998	Invasive	Dijkstra et al., 2009	Escaped from an animal trader near the town of Weert.

Introductions

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Introduced to	Introduced from	Year	Reason	Introduced by	Established in wild through		References	Notes
Introduced to	Introduced from	Year	Reason	Introduced by	Natural reproduction	Continuous restocking	References	Notes
Argentina	Belgium	1973	Ornamental purposes (pathway cause)		Yes		Novillo and Ojeda (2008)	Introduced to Villa Flandria, Buenos Aires
Belgium		2000s	Ornamental purposes (pathway cause)		Yes	No	Stuyck et al. (2009)	Introduced at Dadizele. Ongoing eradication programme.
France		early 1970s	Ornamental purposes (pathway cause)		Yes	No	Jouanin (1986)	Introduced to Cap d'Antibes. Control programme planned.
Japan	Taiwan	1930s	Botanical gardens and zoos (pathway cause)		Yes		Udagawa (1954)	They escaped from the zoo and became naturalised on Izu-Oshima Island
Japan	Taiwan	1950s	Botanical gardens and zoos (pathway cause)		Yes		Ono (2001)	Introuced to Kanagawa, Japan. Escaped from Enoshima Zoo in the 1950s and Nogeyama Zoo in the 1960s. Released pets were also included
Japan		1970s			Yes			Introduced to Shizuoka
Japan		1936	Botanical gardens and zoos (pathway cause)		Yes			Introduced to Gifu, Japan. In 1936, individuals reared for an exhibition escaped
Japan		1970s	Intentional release (pathway cause)		Yes			Introduced to Osaka; established but rare
Japan	Japan	1954	Botanical gardens and zoos (pathway cause)		Yes		Setoguchi (1990)	In 1954, 100 squirrels were moved from Izu-Oshima Island to Tomogashima Island, Wakayama
Japan		1970s	Intentional release (pathway cause)		Yes			Introduced to Hyogo. 10 squirrels were released; small population established
Japan		1986			Yes			Introduced to Fukue Island, Nagasaki
Japan		1999	Botanical gardens and zoos (pathway cause)		Yes			Introduced to Iki Island, Nagasaki
Japan		2008			Yes			Introduced to Kumamoto. Small population established
Japan		1955						Introduced to Takashima Island
Netherlands		1998	Pet trade (pathway cause)				Dijkstra et al. (2009)	Introduced near Weert.

Risk of Introduction

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Callosciurus species are often traded in local markets in South-East Asia, the original range. Export and import of these species for ornamental uses and pet trades ought to be prohibited by law, because they easily escape from their cages.

Habitat

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C. erythraeus is found in various types of wooded habitat (natural forests, conifer plantations, orchards, bushes and city parks), but it prefers mixed species broad-leaved evergreen forests in Japan (Okubo et al., 2005) and France (Gerriet, 2009). Mean home range size is small, varying from 0.3 ha to 0.5 ha in females and from 1.4 ha to 2.2 ha in males (Tamura et al., 1989). In a woody area near Cap d’Antibes, France, the mean annual home range size determined by radiotracking varied from 3.2 ± 0.5 ha (n=7) for females to 8.1 ± 1.3 ha (n=6) for males (95% Fixed Kernel method: A. Dozières, Muséum National d'Histoire Naturelle, Paris, France, unpublished). Home ranges overlap between individuals (Tamura et al., 1989; A. Dozières, unpublished).

Habitat List

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Category	Sub-Category	Habitat	Presence	Status
Terrestrial

	Terrestrial – Managed	Cultivated / agricultural land	Present, no further details	Harmful (pest or invasive)
		Cultivated / agricultural land	Present, no further details	Natural
		Managed forests, plantations and orchards	Secondary/tolerated habitat	Harmful (pest or invasive)
		Managed forests, plantations and orchards	Secondary/tolerated habitat	Natural
		Disturbed areas	Present, no further details	Harmful (pest or invasive)
		Disturbed areas	Present, no further details	Natural
		Urban / peri-urban areas	Present, no further details	Harmful (pest or invasive)
		Urban / peri-urban areas	Present, no further details	Natural
	Terrestrial ‑ Natural / Semi-natural	Natural forests	Principal habitat	Harmful (pest or invasive)
		Natural forests	Principal habitat	Natural
		Scrub / shrublands	Present, no further details	Harmful (pest or invasive)
		Scrub / shrublands	Present, no further details	Natural

Biology and Ecology

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Genetics

Chromosomes: 2n=40 (Oshida and Yoshida, 1999).

Reproductive Biology

Breeding occurs throughout the year in Taiwan, Japan and France (Tamura et al., 1989; Gurnell and Wauters, in Mitchell-Jones et al., 1999). Nine to 17 males gather near the oestrous female and mate according to their dominance ranks (Tamura et al., 1988). Individual females breed 0-3 times a year with a mean of 1.9 times in Taiwan and 1.2 times in Japan. The number of embryos is 1.8 (mean value) in Taiwan (T’sui et al., 1982), 1-4 with a mean of 2.3 in Japan (Tamura, 1999), and 1.8 ± 0.1 (n=19) in France (J. L. Chapuis, Muséum National d'Histoire Naturelle, Paris, France, unpublished). The mean number of weaned young per litter is 1.1 in Taiwan and 1.3 in Japan. The gestation period is 47-49 days in captivity (Tamura, 1999).

Life span

Both males and females mature at less than 1 year old; young individuals disperse from their natal areas and usually establish their own home ranges when about 1 year old. In Japan, 43% of adult males live for more than 1 year after reaching this stage, 35% for 2 years, and 10% for 3 years, but none for more than 5 years; 81% of adult females live for more than 1 year, 66% for 2 years, 11% for 4 years, and none for more than 5 years. In Taiwan, 32% of adult males live for more than 1 year, and only 15% for 2 years; 34% of adult females live for more than 1 year, and only 20% for more than 2 years (Tamura et al., 1989).

Nutrition

C. erythraeus eats various parts (leaves, buds, flowers, fruits, seeds, and bark) of various species of plant, as well as fungi, and animal materials such as insects, bird eggs and snails (Chou et al., 1985, Ozaki, 1986; Tamura et al., 1989; Setoguchi, 1990).

Environmental Requirements

This species is inactive in the morning when the temperature is less than 0°C in Kanagawa, Japan (Yamamoto and Tamura, 2006). It is observed foraging at midday, the warmest time of the day, in cold seasons. The northern edge of the distribution range at China (the original habitat) coincides with the line where mean annual temperature is 14°C.

Climate

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Climate	Status	Description
Af - Tropical rainforest climate	Tolerated	> 60mm precipitation per month
Am - Tropical monsoon climate	Tolerated	Tropical monsoon climate ( < 60mm precipitation driest month but > (100 - [total annual precipitation(mm}/25]))
As - Tropical savanna climate with dry summer	Tolerated	< 60mm precipitation driest month (in summer) and < (100 - [total annual precipitation{mm}/25])
Aw - Tropical wet and dry savanna climate	Tolerated	< 60mm precipitation driest month (in winter) and < (100 - [total annual precipitation{mm}/25])
Cf - Warm temperate climate, wet all year	Preferred	Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year
Cs - Warm temperate climate with dry summer	Preferred	Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers
Cw - Warm temperate climate with dry winter	Preferred	Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)

Air Temperature

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Parameter	Lower limit	Upper limit
Mean annual temperature (ºC)	14

Natural enemies

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Natural enemy	Type	Life stages	References
Brevistriata callosciuri	Parasite		Matsudate et al., 2003
Butastur indicus	Predator	Adult Female/Adult Male	Tamura, 2009
Buteo buteo	Predator	Adult Female/Adult Male	Tamura, 2009
Ceratophyllus anisus	Parasite		Shinozaki et al., 2004a
Elaphe	Predator	Juvenile	Tamura, 2009
Enderleinellus kumadai	Parasite		Kano and Shinonaga, 1997; Shinozaki et al., 2004a; Shinozaki et al., 2004b
Felis bengalensis	Predator	Adult Female/Adult Male	Tamura, 2009
Felis catus	Predator	Adult Female/Adult Male	Tamura, 2009
Haemaphysalis flava	Parasite		Shinozaki et al., 2004a
Hoplopleura erismata	Parasite		Dozières et al., 2010
Martes flavigula	Predator	Adult Female/Adult Male	Tamura, 2009
Neohaematopinus callosciuri	Parasite		Kano and Shinonaga, 1997; Shinozaki et al., 2004a; Shinozaki et al., 2004b
Spilornis cheela	Predator	Adult Female/Adult Male	Tamura, 2009
Strongyloides	Parasite		Matsudate et al., 2003
Trimeresurus	Predator	Juvenile	Tamura, 2009

Notes on Natural Enemies

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Predators: The main predators are carnivorous mammals (e.g. Martes flavigula, Felis bengalensis), snakes (e.g. Trimeresurus sp. and Elaphe sp.) and hawks (e.g., Spilornis cheela, Butastur indicus) in China and southeast Asia, and domestic cats (Felis catus), snakes (e.g. Elaphe climacophora) and hawks (e.g., Buteo buteo) in Japan. C. erythraeus emits different alarm vocalizations in response to three different types of predator, namely carnivores, snakes and hawks (Tamura, 2009).

Parasites: C. erythraeus is parasitized in Japan by the flea Ceratophyllus anisus, the lice Enderleinellus kumadai and Neohaematopinus callosciuri, and the tick Haemaphysalis flava (Kano and Shinonaga, 1997; Shinozaki et al., 2004a, b; Tamura, 2009). Two parasitic helminths, Brevistriata callosciuri and Strongyloides sp., are also recorded in Japan (Matsudate et al., 2003). In France and Belgium, the macroparasite fauna is dominated by the sucking louse E. kumadai (in Belgium also by Hoplopleura erismata), and very few intestinal worms accidentally acquired from local fauna in both countries (Dozières et al., 2010).

Means of Movement and Dispersal

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Most introductions of C. erythraeus have been for ornamental purposes or presentation in zoos and botanical gardens. However, the pet trade should not be ignored.

C. erythraeus is mainly arboreal and often uses electric wires and hedgerows for locomotion in urban areas of Japan and in France. It is active in the early morning and evening in Taiwan (Chou et al., 1985).

Pathway Causes

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Cause	Long Distance	References
Botanical gardens and zoos	Yes	Ono, 2001; Udagawa, 1954
Escape from confinement or garden escape	Yes	Jouanin, 1986; Jouanin, 1992
Ornamental purposes	Yes	Novillo and Ojeda, 2008
Pet trade	Yes	Dijkstra et al., 2009; Ono, 2001

Impact Summary

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Category	Impact
Cultural/amenity	Positive and negative
Economic/livelihood	Negative
Environment (generally)	Negative

Economic Impact

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On Izu-Oshima Island, Japan, Camellia seeds, an important agricultural product, are severely damaged, and consequently many farmers gave up their production. Debarking in conifer plantations causes serious economic damage in Taiwan and Japan (Kuo, 1985; Torii, 1993); the damage rate was 80-90% in artificial forests of Chamaecyparis obtusa in Shizuoka and Nagasaki, Japan (Torii, 1993). Wooden shutter boxes and eaves are often damaged, and the squirrels make holes in them for their nests. Electric and telephone wires are cut.

Environmental Impact

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Impact on Habitat

C. erythraeus in Japan causes severe debarking of trees in winter when short of other foods. Natural forests have suffered considerable damage when squirrel density has increased.

Impact on Biodiversity

Competition for food and nest sites is a concern. C. erythraeus is known to predate animal materials including bird eggs, insects, and snails (Tamura et al., 1989). The native Japanese squirrel species, Sciurus lis, is locally declining (Ministry of the Environment, Japan, 2002), as is probably the case in France for the European red squirrel Sciurus vulgaris ( A. Dozières, J.L. Chapuis, Muséum National d'Histoire Naturelle, Paris, France, unpublished).

Threatened Species

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Threatened Species	Conservation Status	Where Threatened	Mechanism	References	Notes
Sciurus lis	National list(s) National list(s)		Competition - monopolizing resources	Ministry of the Environment, 2002
Sciurus vulgaris	LC (IUCN red list: Least concern) LC (IUCN red list: Least concern)		Competition - monopolizing resources

Social Impact

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Cultural assets such as wooden traditional houses and statues are damaged.

Risk and Impact Factors

Top of page Invasiveness

Proved invasive outside its native range
Has a broad native range
Abundant in its native range
Highly adaptable to different environments
Capable of securing and ingesting a wide range of food
Gregarious

Impact outcomes

Damaged ecosystem services
Ecosystem change/ habitat alteration
Infrastructure damage
Negatively impacts agriculture
Negatively impacts cultural/traditional practices
Negatively impacts forestry
Reduced native biodiversity
Threat to/ loss of native species

Impact mechanisms

Competition - monopolizing resources
Predation

Likelihood of entry/control

Highly likely to be transported internationally deliberately
Difficult/costly to control

Uses

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Social Benefit

C. erythraeus has often been used as an ornamental species and a tourist attraction. People enjoy contact with the squirrels, but they do not understand the problems caused by invasive species.

Uses List

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Environmental

Amenity

General

Botanical garden/zoo
Pet/aquarium trade

Detection and Inspection

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The presence of C. erythraeus is indicated by: (1) its distinctive pattern of bark stripping; (2) its distinctive sound, like a dog barking (Tamura, 1995); and (3) direct sightings.

Similarities to Other Species/Conditions

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It is difficult to distinguish C. erythraeus from other species of the same genus; for example, some forms have the entire ventral pelage agouti as in C. caniceps, and some have a reddish brown dorsum as in some types of C. finlaysonii. None of the species in this genus have ear tufts at any season.

Prevention and Control

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Eradication

A programme is under way to eradicate the C. erythraeus population at Dadizele, Belgium (Stuyck et al., 2009).

Control

On Izu-Oshima and Fukue Islands and in Shizuoka and Kanagawa Prefectures, Japan, population control using traps has been conducted, because the population density of C. erythraeus became high enough to cause agroforestry damage. However, it is difficult to eradicate the species once it has become established. In a similar situation in France, a control programme is planned at Cap d'Antibes, France, starting in 2011 (J.L Chapuis, Muséum National d'Histoire Naturelle, Paris, France, personal communication, 2010).