Red-toothed shrews (Soricinae)
Class: Mammalia
Order: Insectivora
Family: Soricidae
Subfamily: Soricinae
Thumbnail description
Small mouse-like mammals with long pointed snouts, short legs, and small eyes
Size
1.5–5.3 in (4.0–13.5 cm); 0.06–1.5 oz (2–40 g)
Number of genera, species
11 genera; 122 species
Habitat
Cold and wet environments, forests, banks of rivers and streams, exceptionally also warm and arid habitats
Conservation status
Critically Endangered: 5 species; Endangered: 8 species; Vulnerable: 7 species; Lower Risk/Near Threatened: 3 species; Data Deficient: 1 species
Distribution
Temperate zone in the Northern Hemisphere, Indo-Malaysia, Central America, and the northernmost parts of South America
Evolution and systematics
Shrews (Soricidae) are small mammals with rather unspecialized body plans, retained almost unchanged since they evolved about 45 million years ago (mya). The family is usually divided into a number of extinct and extant subfamilies. The two extant subfamilies are the Crocidurinae and the Soricinae. The members of the subfamily Soricinae, redtoothed shrews, are further subdivided into seven tribes, one of them extinct (Anourosoricini, Beremendiini, Blarinellini, Blarinini, Neomyini, Notiosoricini, and Soricini). The delimitation of some tribes of the subfamily Soricinae is still open to discussion. The genetic distances among different genera of soricines based on allozyme variation generally support a subdivision of the living species into the tribes. Species of soricine shrews may show considerable chromosomal and genetic differentiation. Karyotypic and protein electrophoresis studies have been very helpful in identifying many sibling and cryptic species that were difficult to recognize by conventional methods.
According to the number of the tribes and genera included, the Soricinae constitute the most diverse subfamily among shrews. Their fossil record comes from Eurasia, Africa, and North America. The fossil remains are still insufficiently studied, and many gaps exist in our knowledge. The oldest soricines have been reported from the early Miocene of North America about 24 mya (Antesorex), and the Holarctic region in the Northern Hemisphere is considered the area of origin of this lineage. The species richness in the fossil record remained low in the Tertiary and during the Early and Middle Pleistocene. In the Late Pleistocene a plethora of forms appeared in Europe, Asia, and North America. The large number of living taxa unrepresented by late Pleistocene records suggests that we have only a minute sample of the total number of species that have occurred in the past. From North America, the soricine shrews spread into the extreme northern parts of South America, and from Europe and Asia to tropical regions of Indo-Malaysia. Soricines are almost completely absent from Africa, except for one extinct species, Asoriculus maghrebensis.
Shrews have played an important role in reconstructing faunal, floral, and climatic changes within various continents. Occurrence of specifically identifiable fossil remains allows mapping of environmental changes through time. This is particularly striking in regard to Pleistocene faunas, where massive rearrangements of the geographical distribution of shrews can be followed and allow reconstruction of vegetation and climatic changes.
Physical characteristics
Soricine shrews are small mouse-sized insectivores with a pointed snout, short legs, and usually a long tail. The smallest soricines (Sorex minutissimus, Sorex hoyi) have a body mass of 0.07–0.1 oz (2–3 g), and are among the smallest known mammals. The size of the largest soricines slightly exceeds that of the house mouse. The largest representatives of the subfamily, water shrews of the genus Chimarrogale, weigh up to 1.5 oz (40 g), their head and body length ranges up to 5.3 in (13.5 cm), while tail length can be up to 5 in (12.5 cm). They walk on the soles of their feet, which have five clawed digits. The eyes are extremely small and their sight is poor, but the sense of smell is keen as indicated by long, mobile snouts. The external ears are usually hidden in their fur. Pelage is usually dark, with brown, grayish, or black coat color. The skull is narrow and elongated, and the brain is small and smooth, dominated by large olfactory bulbs.
Certain skeletal and dental characters are diagnostic for the subfamily: the articulation of the mandibular condyle, the position of the mental foramen, and the morphology of the lower premolar. The dentition is highly specialized and similar from species to species. They have continuous rows of teeth classified as incisors, antemolars, premolars, and molars. Homologies of the antemolars are difficult to determine and thus, the dental formula is expressed using different terms than in other mammals. The number of antemolars is the only difference seen between living species in the dental formulae. Part of dental variation in soricines is clearly correlated with ecological adaptations.
In most of the Soricinae, a reddish, iron-containing pigmentation on cusps of their teeth is present. The function of tooth pigmentation is not yet clearly understood, but it is supposed that pigmented enamel should be harder than unpigmented and should provide a protection against abrasion. The intensity of pigmentation varies. Some species (Blarina, Blarinella, Sorex daphaenodon) have a very strong dark pigmentation, other species (Anourosorex, Chimarrogale, Nectogale) appear to have reduced red enamel or even unpigmented teeth. The absence of tooth pigment may also be explained by ecological, particularly dietary, factors.
Distribution
The subfamily Soricinae seems to be of Holarctic origin and likely evolved in a temperate climate. This is reflected in the pattern of present day distribution. Soricines inhabit most of the temperate and arctic parts of the Northern Hemisphere in Europe, Asia, and North America. In the New World, they occur also in Mexico and Central America and a single genus (Cryptotis) inhabits the mountain ranges of the Andes in northern South America. In the Old World the only soricines occurring in the tropics are members of several genera endemic to Southeast Asia (Anourosorex, Chimarrogale, and Soriculus).
Habitat
Soricines usually inhabit cool and moist areas in forests of various types. They are mainly terrestrial, but some take to water freely, and others burrow a little. They are usually abundant wherever there is sufficient ground vegetation to provide cover. They occur over a great altitudinal range and in many kinds of plant communities. They prefer moist habitats, but some species are found also in arid regions (Notiosorex). Other species of soricines inhabit banks of rivers, streams, and lakes, and are modified for an aquatic or semiaquatic life. Soricine shrews live mainly in areas with distinct seasonal changes in weather and habitat, often in areas with extreme low temperatures in winter. An adequate snow cover ensures stability and a relatively mild subnivean (under snow) microclimate.
Behavior
Shrews live hidden under cover and mostly lead nocturnal lives. Their prey does not require group hunting and solitary foraging prevails. Predation avoidance in soricines does not depend on a long-distance escape but rather on finding shelter. Soricines live solitarily and they are territorial almost all their life. Their strict territoriality is promoted by exploitation of scarce and evenly distributed resources. Shrews establish large territories within which most foraging and nesting, as well as courtship and mating, take place. In autumn and winter, territories are maintained to maximize survivorship, and in spring and summer, to maximize reproduction. The maintenance and defense of territories is based on acoustic and olfactory communication, but direct aggression involving combat and biting is also frequent. With respect to the distribution of food resources and their predictability, two social systems of territorial behavior have been described in soricine shrews—stable and shifting territories.
The shrews with stable territories do not nest communally in order to conserve heat by huddling and they may be categorized as winter-solitary species. In spring, the territories enlarge considerably and the territories of opposite sexes may partly overlap. Different males may have different territorial behavior and mating patterns and strategies at the same time and within the same habitat. Long-distance wandering males have a lower reproductive success and they probably suffer higher predation rates. However, their movements are very important because they facilitate gene flow within the species. Courtship and mating last only a short period. Nevertheless, a female can copulate with several males during this short time and multiple paternity of pups within one litter may occur. This female strategy can reduce inbreeding. The mating system is thus rather promiscuous.
The system of shifting territories is typical for semi-aquatic shrews (Chimarrogale, Nectogale, Neomys, Sorex palustris, Sorex bendirii). In these species, the exploitation of food resources is clumped in space and undergoes unpredictable changes that do not favor strong and stable territoriality. Territories are not maintained for the whole life, and semi-aquatic shrews usually shift along banks of flowing waters and water reservoirs, so that their territories are changed every few weeks or months. The mating system of shrews with shifting territories is promiscuous, and the breeding females are the most aggressive members of populations. The dissimilarity of social systems of certain species (Notiosorex, Cryptotis) to those of other soricines can be related to the fact that they inhabit regions with relatively warm climates and/or with poor food resources.
Reactions of soricines with stable territories to shrews of other species, being potential competitors, are also agonistic, including the larger shrews preying upon the smaller species. In interspecific competition, behavior leading to mutual avoidance of the individuals plays a more important role than direct aggression.
Feeding ecology and diet
Shrews feed mainly on soil invertebrates and as a whole may be seen as opportunistic and generalized invertebrate feeders, although some partitioning may occur among syntopical species. No extreme specialist occurs, even though some shrews are more or less aquatic, which also is reflected in their diet. The fossil species Arctosorex polaris from the late Neogene of Ellesmere Island might be the only shrew specialized for frugivory.
Sorex shrews form a well-defined guild of insectivorous mammals with opportunistic feeding habits and largely over-lapping resource requirements. In a guild, up to six species may occur together in the same time and place. Competition is likely to be common in such a case. Major differences in dietary composition and foraging mode reflect body size in shrews. Small species are often epigeal, feed mainly on arthropods, and have a relatively narrow niche breadth. Large species are usually hypogeal, and feed on earthworms and other soil-dwelling invertebrates. Body size thus plays an important role in ecological separation in multi-species assemblages of terrestrial soricine shrews. Assemblages of shrews in boreal forests show a shift from the dominance of small species in unproductive habitats to the dominance of large species in productive habitats.
Shrews have two features in common that influence their whole energetic design: a small body size and an insectivorous food habit. They do not hibernate in winter and, with few exceptions, they are not able to enter torpor. The soricines have very high basal rates of metabolism and they maintain a high and precisely regulated body temperature. The very high metabolic rates in shrews are markedly higher than would be expected in mammals of their body size (up to 315% of the expected value). Extremely high metabolic rates are characteristic especially for the genus Sorex. The high basal rates of metabolism were attributed to their origin in a temperate climate and to their large litter size. High energy costs of reproduction are apparently associated with high metabolic rates. The high metabolic rates of most soricines make them susceptible to food shortage and result in the requirement of a constant food supply. Starvation time for the genus Sorex varies between five and 10 hours.
Soricine shrews in northern temperate regions undergo a decline in body mass and body size during winter (known as the Dehnel's effect). This is interpreted as an adaptation permitting reduction in food requirements. Winter weight loss in Sorex usually amounts to 25–40%, and it is accompanied by a reduction in the size of the skull and most organs.
Reproductive biology
Seasonal regimes of resource availability favor high fecundity during the flush of resources occurring during summer. Therefore, the reproduction of soricine shrews is strongly seasonal, occurring when food is highly available and weather conditions are optimal. Soricines produce significantly larger litters than crocidurines, on average 5.1 young per litter (5.9 in Sorex), but more than 10 young can also be born in a litter. One female can produce one to four litters per year. Increased reproductive output may be a major advantage derived from the high rate of metabolism in many soricines.
Evidence from the field and laboratory studies suggests that female shrews of a variety of species show a tendency to mate with many different males. Multiple paternity in the litter of wild-caught females has been demonstrated in the promiscuous common shrew, with up to six different fathers per litter. Most soricines have a short gestation period (on average 21 days) and a longer weaning period. Young are born in a very early stage of development and are among the most altricial placental mammals. The pups develop quickly, and usually they are weaned within three to four weeks. After the final break of mother-offspring bond, the young leave the nest and their dispersal begins. Juvenile shrews usually do not reproduce during their first summer because generally they mature in the next spring. High social intolerance and aggressiveness with increased population density are important factors inhibiting the maturation and reproduction of juveniles. After reproduction, and as the autumn approaches, the parental population quickly dies. The average life-span of a reproducing soricine shrew is 14.7 months.
Conservation status
The soricine shrews included in the 2002 IUCN Red List often belong to very rare and endemic species with restricted distribution and low population densities. Some of the threatened species are only known from the locality of their original description. However, the major threat for the soricine shrews is environmental disturbance and pollution. Loss of forest habitats has a considerable effect on forest-dwelling species. The rate of deforestation taking place in south and Southeast Asia is an apparent reason for including several soricine species from this particular geographic region among the category of Critically Endangered. Similar threats may arise in other regions from human interference with wetlands and from freshwater pollution. Shrews are exceptionally susceptible to accumulation of heavy metals in their tissues through their diet consisting of large amounts of earthworms. Long-term persistence of DDT has also been reported in soricine shrews.
Conservation of soricine shrews is only possible if it is fully integrated with the broader issues of environmental management and sustainable development. Furthermore, there is an urgent need for considerable research because important information is still lacking for many species.
Significance to humans
Soricine shrews are an important component of natural communities and ecosystems and they have an important ecological role. The impact of soricines upon the natural environment, whether through the large amount of invertebrates consumed, or their role as prey species for many predators, is considerable. Shrews have a significant impact on litter decay, and they diminish the population density of soil invertebrates thus increasing their productivity. In this way, soricine shrews in temperate habitats accelerate decomposition of forest litter and organic matter in the upper soil layer. They can play a role in natural control of various insect pests.
Accumulation of heavy metals in insectivorous mammals through their diet containing earthworms is extremely high, and the burden in tissues of shrews may be used as a useful indicator of environmental contamination. It is unknown whether shrews have a greater resistance to heavy metals than other mammals. Strong effects of rapid environmental change on developmental stability were also recorded in free-living populations of soricine shrews and provided a tool to monitor changes in natural environments. Shrews are becoming favorable model species in research of various issues of biomedicine and evolutionary biology.
Species accounts
Mole-shrewChinese short-tailed shrew
Northern short-tailed shrew
American least shrew
Eurasian water shrew
Himalayan water shrew
Elegant water shrew
Hodgson's brown-toothed shrew
Desert shrew
Alpine shrew
Common shrew
Eurasian pygmy shrew
Giant shrew
American pygmy shrew
American water shrew
Resources
Books:Corbet, G. B., and J. E. Hill. The Mammals of the Indomalayan Region: A Systematic Review. Oxford: Oxford University Press, 1992.
Eurasian Insectivores and Tree Shrews—Status Survey and Conservation Action Plan. Compiled by David Stone and the IUCN/SSC Insectivore, Tree Shrew and Elephant Shrew Specialist Group. Gland, Switzerland: IUCN, 1995.
Mitchell-Jones, A. J., et al. The Atlas of European Mammals. London: Poyser Natural History-Academic Press, 1999.
Wilson, D. E., and S. Ruff, eds. The Smithsonian Book of North American Mammals. Washington, DC: Smithsonian Institution Press, 1999.
Wójcik, J. M., and M. Wolsan, eds. Evolution of Shrews. Bialowieza, Poland: Mammal Research Institute, Polish Academy of Sciences, 1998.
Organizations:IUCN Species Survival Commission, Insectivore Specialist Group, Dr. Werner Haberl, Chair. Hamburgerstrasse 11, Vienna, A-1050 Austria. Phone: +4315861094. Fax: +4315861094. E-mail: shrewbib@sorex.vienna.at Web site:
[Article by: Jan Zima, PhD]
