7
Nutrient Requirements of the Vole

It has been demonstrated that voles are useful as a small-animal model for testing the quality of forages and other agricultural crops (Elliot, 1963; Keys and Van Soest, 1970; Shenk et al., 1971; Shenk et al., 1974, 1975; Shenk, 1976). More recently, laboratory and field research on voles has focused on the effect of nutritional and other environmental factors on reproduction and population growth (e.g., Cole and Batzli, 1979; Nelson et al., 1983; Batzli, 1985, 1986; Hasbrouck et al., 1986; Spears and Clarke, 1987; Hall et al., 1991). In nature, voles undergo significant annual and cyclical changes in population density that are not fully understood (Taitt and Krebs, 1985). Despite the ecological importance of voles and their apparent responsiveness to nutritional variables, little is known about the nutrient requirements of these abundant rodents.

BIOLOGICAL CHARACTERISTICS

Voles (Microtus sp.) represent a successful radiation of small herbivores that are particularly abundant in grassy areas in Asia, Europe, and North America. The genus Microtus encompasses about 60 species, if Pitymys is accepted as a subgenus of Microtus (Corbet and Hill, 1980; Nowak and Paradiso, 1983; Anderson, 1985). The most common species for laboratory study in North America are the prairie vole (M. ochrogaster ), the meadow vole (M. pennsylvanicus), and the pine vole [M. (Pitymys) pinetorum].

Taxonomically, voles are members of the rodent subfamily Microtinae (sometimes called Arvicolinae) that includes lemmings, muskrats, and nutria (Anderson, 1985). Other microtine genera also are referred to as voles, such as redbacked voles (Clethrionymys sp.), mountain voles (Alticola sp.), and water voles (Arvicola sp.). It is not known if the nutritional requirements of these genera differ from Microtus, but because of differences in natural diet, body size, and physiological adaptations to the environment (Batzli, 1985; Woodall, 1989) they will not be included in this discussion.

In nature, voles rely on grasses both for shelter and as a primary food source (Getz, 1985). Although all Microtus consume primarily the vegetative parts of plants, the types of plants eaten vary among species, habitats, and seasons (Batzli, 1985). It seems that voles select food plant species on the basis of availability, composition (particularly nitrogen and fiber fractions), and deterrent secondary compounds such as phenolics and tannins (Batzli, 1985; Lindroth et al., 1986; Marquis and Batzli, 1989; Bucyanayandi and Bergeron, 1990). Unlike many small rodents, voles remain active in winter months—tunneling under snow, if necessary, and feeding on senescent grasses, rhizomes, seeds, and other plant material (Batzli, 1985; Getz, 1985). Ability to survive in cold conditions on foods of low digestible energy content appears to be a key adaptive feature of voles (Wunder, 1985; Hammond and Wunder, 1991).

Rapid reproductive rates are also characteristic of voles when food is abundant. Because female voles typically enter into estrus and are inseminated shortly after giving birth, concurrent pregnancy and lactation are common, leading to the production of litters at about 3-week intervals (Kudo and Oki, 1984; Keller, 1985). Developmental and reproductive indices of some of the common laboratory voles, as well as scientific binomials of the species discussed in this chapter, are listed in Table 7-1. Most of the data in Table 7-1 are from laboratory colonies maintained on natural-ingredient diets and presumably represent animals at a high plane of nutrition. Postnatal growth rates were measured in the first weeks postpartum; daily growth rates after weaning can be expected to be similar or somewhat greater. For example, Shenk (1976) considered a weanling growth rate of 0.9 to 1.1 g/day to be maximal and indicative of dietary adequacy in meadow voles; preweaning growth rates in this species average about 0.7 g/day (Table 7-1).



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Nutrient Requirements of Laboratory Animals: Fourth Revised Edition, 1995 7 Nutrient Requirements of the Vole It has been demonstrated that voles are useful as a small-animal model for testing the quality of forages and other agricultural crops (Elliot, 1963; Keys and Van Soest, 1970; Shenk et al., 1971; Shenk et al., 1974, 1975; Shenk, 1976). More recently, laboratory and field research on voles has focused on the effect of nutritional and other environmental factors on reproduction and population growth (e.g., Cole and Batzli, 1979; Nelson et al., 1983; Batzli, 1985, 1986; Hasbrouck et al., 1986; Spears and Clarke, 1987; Hall et al., 1991). In nature, voles undergo significant annual and cyclical changes in population density that are not fully understood (Taitt and Krebs, 1985). Despite the ecological importance of voles and their apparent responsiveness to nutritional variables, little is known about the nutrient requirements of these abundant rodents. BIOLOGICAL CHARACTERISTICS Voles (Microtus sp.) represent a successful radiation of small herbivores that are particularly abundant in grassy areas in Asia, Europe, and North America. The genus Microtus encompasses about 60 species, if Pitymys is accepted as a subgenus of Microtus (Corbet and Hill, 1980; Nowak and Paradiso, 1983; Anderson, 1985). The most common species for laboratory study in North America are the prairie vole (M. ochrogaster ), the meadow vole (M. pennsylvanicus), and the pine vole [M. (Pitymys) pinetorum]. Taxonomically, voles are members of the rodent subfamily Microtinae (sometimes called Arvicolinae) that includes lemmings, muskrats, and nutria (Anderson, 1985). Other microtine genera also are referred to as voles, such as redbacked voles (Clethrionymys sp.), mountain voles (Alticola sp.), and water voles (Arvicola sp.). It is not known if the nutritional requirements of these genera differ from Microtus, but because of differences in natural diet, body size, and physiological adaptations to the environment (Batzli, 1985; Woodall, 1989) they will not be included in this discussion. In nature, voles rely on grasses both for shelter and as a primary food source (Getz, 1985). Although all Microtus consume primarily the vegetative parts of plants, the types of plants eaten vary among species, habitats, and seasons (Batzli, 1985). It seems that voles select food plant species on the basis of availability, composition (particularly nitrogen and fiber fractions), and deterrent secondary compounds such as phenolics and tannins (Batzli, 1985; Lindroth et al., 1986; Marquis and Batzli, 1989; Bucyanayandi and Bergeron, 1990). Unlike many small rodents, voles remain active in winter months—tunneling under snow, if necessary, and feeding on senescent grasses, rhizomes, seeds, and other plant material (Batzli, 1985; Getz, 1985). Ability to survive in cold conditions on foods of low digestible energy content appears to be a key adaptive feature of voles (Wunder, 1985; Hammond and Wunder, 1991). Rapid reproductive rates are also characteristic of voles when food is abundant. Because female voles typically enter into estrus and are inseminated shortly after giving birth, concurrent pregnancy and lactation are common, leading to the production of litters at about 3-week intervals (Kudo and Oki, 1984; Keller, 1985). Developmental and reproductive indices of some of the common laboratory voles, as well as scientific binomials of the species discussed in this chapter, are listed in Table 7-1. Most of the data in Table 7-1 are from laboratory colonies maintained on natural-ingredient diets and presumably represent animals at a high plane of nutrition. Postnatal growth rates were measured in the first weeks postpartum; daily growth rates after weaning can be expected to be similar or somewhat greater. For example, Shenk (1976) considered a weanling growth rate of 0.9 to 1.1 g/day to be maximal and indicative of dietary adequacy in meadow voles; preweaning growth rates in this species average about 0.7 g/day (Table 7-1).

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Nutrient Requirements of Laboratory Animals: Fourth Revised Edition, 1995 TABLE 7-1 Reproductive and Developmental Indices of Voles Species Name Common Name Adult Weight, g Gestation, days Litter Size Birth Weight, g Postnatal Growth, g/day Approx. Weaning Age, Days M. arvalis Common vole 35 20 4.8 2.1 — — M. californianus California vole 50 21 4.7 2.8 1.1 14 M. montanus Montane vole 50 21 6.0 2.5 1.0 15–17 M. montebelli Japanese field vole 41 21 4.7 2.7 0.9 21 M. ochrogaster Prairie vole 40 20–22 3.9 2.8 1.0 14–21 M. oeconomus Tundra vole 45 20.5 4.0 3.0 0.8 18 M. pennsylvanicus Meadow vole 40 20–21 4.4 2.3 0.7 14 M. pinetorum Pine vole 26 24 2.2 2.0 — 17   SOURCES: Lee and Horvath (1969), Richmond and Conaway (1969), Lindroth et al. (1984), Kudo and Oki (1984), Nadeau (1985). HUSBANDRY AND FORM OF DIET Vole colonies are usually founded by the capture of wild animals. Successful breeding colonies have been established for at least 10 species of voles in North America (Mallory and Dieterich, 1985) and several other species in Europe and Japan (Kudo and Oki, 1984). Different colonies of the same species may be genetically distinct because of substantial variation among the founding wild populations. Extensive morphological variation over the ranges of most species has resulted in the description of a plethora of subspecies. At the extreme, 27 subspecies have been described for Microtus pennsylvanicus (Hoffman and Koeppel, 1985). Populations of voles may vary in characteristics such as body mass and litter size, although the extent to which this variation is a result of genetic or environmental effects is not clear (Keller, 1985). Care must be exercised in generalizing from one colony to another; the values listed in Table 7-1 may not apply to all colonies. Voles have been maintained in a variety of cages, but plastic mouse cages with solid bottoms and added bedding material are especially suitable (Richmond and Conaway, 1969; Mallory and Dieterich, 1985). Details of lighting, ambient temperature, social groupings, and other aspects of the husbandry of voles have been reviewed by Lee and Horvath (1969), Richmond and Conaway (1969), Dieterich and Preston (1977), and Mallory and Dieterich (1985). NATURAL-INGREDIENT AND PURIFIED DIETS After an initial adaptation period, voles adapt well to captivity and can be fed on various natural-ingredient diets. Pelleted natural-ingredient diets developed for rabbits, mice, rats, and guinea pigs are apparently the most commonly used diets, either with or without supplementation with succulent foods such as lettuce or apples. Of the 10 species listed by Mallory and Dieterich (1985), 7 have been maintained on rabbit diets and 7 on mouse breeder diets. Sole or heavy use of succulent items (such as barley sprouts, carrots, lettuce, and apples) or of unsupplemented seeds and grains (such as sunflower seed, grass seed, and oats) is not recommended because of the likelihood of unintended mineral or vitamin deficiencies (e.g., Batzli, 1986). Purified diets based on vitamin-free casein, a purified cellulose source, a mixture of starch and sugars, and vitamin and mineral premixes and fed in the form of wafers supported adequate weight gains in short-term (6 to 10 days) experiments with weanling meadow voles as long as the cellulose source was at least 25 percent of the diet (Shenk et al., 1971). This may be too short a period to adequately assess response, however (Lindroth et al., 1984). Both prairie voles and tundra voles exhibited normal growth after weaning when fed either a purified diet (based on 20 percent casein and 40 percent cellulose) or a commercial natural-ingredient diet (formulated for rabbits); but the purified diet subsequently led to greater fat deposition, reduced production of litters, and reduced litter size (Lindroth et al., 1984). Sugawara and Oki (1988) noted that purified diets that contained less than 20 percent casein impaired female fertility in the common vole. It has yet to be demonstrated that a purified diet can maintain long-term reproduction in a breeding colony of voles. DIET DIGESTIBILITY AND INTAKE Voles exhibit a number of anatomical features that are associated with herbivory and fermentation of plant fiber. The cheek teeth are high-crowned and contain a complex array of cusps; the stomach is separated into two compartments, one of which (sometimes termed the esophageal pouch) is lined with stratified squamous epithelium and harbors anaerobic microorganisms; the cecum is enlarged and separated in pockets by projecting isthmuses; the colon is both elongate and arranged into spirals that facilitate particle segregation (Vorontsov, 1979; Kudo and Oki, 1984; Stevens, 1988). Although volatile fatty acids are produced

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Nutrient Requirements of Laboratory Animals: Fourth Revised Edition, 1995 in the esophageal pouch when high-fiber diets are consumed (Kudo and Oki, 1984), most fiber fermentation seems to occur in the colon and cecum. According to Bjornhag (1987), voles and allied microtines utilize a colonic separation mechanism to retain fermentative bacteria, enabling the bacteria to proliferate before being washed out of the colon. Coprophagy is also an important part of the digestive strategy of voles; in a study of meadow and pine voles, prevention of coprophagy resulted in a decrease in energy digestibility (Cranford and Johnson, 1989). When fed natural-ingredient diets, voles have energy digestibilities of about 55 to 75 percent, with the lower digestibilities occurring on high-fiber diets (Cherry and Verner, 1975; Batzli, 1986; Hammond and Wunder, 1991). Energy digestibilities of various forages are even more varied and may be less than 50 percent with some grasses (Batzli, 1986; Batzli and Cole, 1979; Johanningsmeier and Goodnight, 1969). The rapid transit of digesta (≈ 12-hour turnover time) precludes extensive fiber digestion. For example, Hammond and Wunder (1991) found neutral detergent fiber (NDF) and acid detergent fiber (ADF) digestibilities of 17 to 18 percent and 6 to 9 percent, respectively, when meadow voles were fed a diet containing 16 percent NDF and 8 percent ADF. However, when fiber fractions were increased (to 39 percent NDF and 23 percent ADF), fiber digestibilities also increased, suggesting some adaptation of digestive function. Voles are able to compensate for an increase in dietary fiber concentrations by an increase in mass of the gastrointestinal tract and especially the cecum (Gross and Wang, 1985; Hammond and Wunder, 1991). Food intake is affected by both energy requirements and digestible energy content of the diet. For example, the daily dry matter intake of adult prairie voles was 13 percent of body weight when they were fed low-fiber (about 8 percent ADF) diets and maintained at an ambient temperature of 23° C, but when fiber was increased to 23 percent ADF and temperature reduced to 5° C, dry matter intake rose to 32 percent of body weight (Hammond and Wunder, 1991). The corresponding digestible energy intakes were about 175 kcal/BWkg0.75/day (732 kJ/BW kg0.75/day) and 370 kcal/BWkg0.75/day (1,548 kJ/BWkg0.75/day). Dry matter and energy intakes of female voles more than double during lactation (Migula, 1969; Innes and Millar, 1981). PROTEIN AND AMINO ACIDS A limited amount of research has been conducted on the growth responses of weanling voles to dietary protein. Shenk et al. (1970) fed weanling meadow voles purified diets containing 3 to 25 percent casein and various proportions of carbohydrates, oil, and cellulose. Voles consuming diets of 9 percent casein (8.3 percent crude protein) or less had subnormal growth rates, whereas voles consuming diets of 12 percent or more casein (11 percent or more crude protein) and intermediate energy densities had apparently normal growth rates (≥0.9 g/day). Sugawara and Oki (1988) observed decreased growth in weanling common voles fed 5 percent casein in a purified diet, as compared to diets containing 10, 15, and 20 percent casein. Spears and Clarke (1987) found no difference between growth rates of field voles fed closed-formula natural-ingredient diets containing 8, 16, and 24 percent protein, but the growth rates of all animals were apparently depressed (≈0.3 g/day); animals fed a 4 percent protein diet gained less than 0.2 g/day. Although these studies indicate that low-protein concentration decreases growth rate, they do not permit a quantitative assessment of the minimum protein requirement of voles, in part because the amino acid patterns may not be ideal. Shenk (1976) asserted that maximal growth of weanling meadow voles could be achieved with purified diets containing mixtures of amino acids providing 13 percent of dry matter as protein and 0.9, 3.2, and 5.9 percent of protein as tryptophan, methionine, and lysine, respectively. Unfortunately these experiments were never published, but unpublished tables provided by Shenk (personal communication, 1989) indicate that the concentrations of amino acids tested, as a percent of total protein, were 0.2, 0.5, 0.9, and 1.3 percent tryptophan; 0.5, 1.2, 3.2, and 5.2 percent methionine; and 0.9, 1.9, 5.9, and 9.9 percent lysine. Given that animals receiving 0.5 percent tryptophan and 1.2 percent methionine had adequate growth rates (0.91 g/day), and that detailed methods and statistics were not reported, this study must be considered preliminary. Animals receiving 0.9, 3.2, and 5.9 percent of protein as tryptophan, methionine, and lysine, respectively, but only 7 percent of dry matter as protein, had somewhat lower rates of growth (0.79 g/day). On the basis of available data, it seems that 11 to 13 percent of high-quality protein is sufficient for maximal weanling growth; however, such diets have not supported maximal reproduction. Sugawara and Oki (1988) noted higher fertility for common voles fed a purified diet containing 20 percent casein than for voles fed diets containing 10 and 15 percent casein. Further study is needed to determine whether higher protein concentrations are required by voles for reproduction than for growth. MINERALS The few studies of mineral metabolism in voles have been stimulated by apparent mineral imbalances in natural foods. Batzli (1986) demonstrated that reproductive performance of California voles was impaired when the voles were fed solely seeds of ryegrass (Lolium sp.) containing

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Nutrient Requirements of Laboratory Animals: Fourth Revised Edition, 1995 0.017 to 0.018 percent calcium and 0.01 to 0.02 percent sodium. Supplementation with sodium chloride improved the frequency and size of litters, but survival and growth of suckling pups were low. Supplementation with calcium chloride did not affect litter frequency or size but did improve postnatal growth and survivorship. When both salts were supplemented, reproductive performance (including postnatal growth and survival) was normal (Batzli, 1986). Thus deficiencies of both sodium and calcium impair reproduction but in different ways. As the amounts of supplements consumed were not determined, it is not possible to estimate requirements. Many of the plants consumed by meadow voles are low in sodium and high in potassium concentrations, especially in spring (Hastings et al., 1991). It has been shown that both low dietary sodium (0.001 percent) and high potassium (≥3.0 percent) concentrations induce hypertrophy of the zona glomerulosa of the adrenal gland of this species (Christian, 1989; Hastings et al., 1991) but actual intakes by wild voles have not been measured. In experimental trials adult (≥20 g), singly housed meadow voles consumed diets containing up to 2.8 percent potassium for 4 weeks without adverse results (Mickelson and Christian, 1991). In the absence of direct estimates of the mineral requirements of voles, and in view of the fact that voles have been successfully maintained when fed diets formulated for rats, mice, and rabbits, it is suggested that diets for voles should contain mineral concentrations similar to those that have proven adequate for these species. VITAMINS Nothing is known about the vitamin requirements of voles other than that both the meadow vole and prairie vole have substantial hepatic activity of l-gulonolactone oxidase (Jenness et al., 1980) and hence do not appear to require a dietary source of ascorbic acid. The fact that colonies of various species of voles have been maintained successfully on natural-ingredient diets formulated for rabbits, rats, and mice suggests that supplementation concentrations of vitamins used for these species may be adequate. REFERENCES Anderson, S. 1985. Taxonomy and systematics. Pp. 52-83 in Biology of New World Microtus, Special Publication No. 8, R. H. Tamarin, ed. Provo, Utah: American Society of Mammologists. Batzli, G. O. 1985. Nutrition. Pp. 779-811 in Biology of New World Microtus, Special Publication No. 8 , R. H. Tamarin, ed. Provo, Utah: American Society of Mammologists. Batzli, G. O. 1986. Nutritional ecology of the California vole: Effects of food quality on reproduction. 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