Genetic control of enzyme polymorphisms in the California vole,Microtus californicus

Inheritance of 15 polymorphic isozymes was investigated in captive Microtus californicus. Eleven of the isozymes show patterns consistent with a Mendelian model of inheritance: glycerol-3-phosphate dehydrogenase (GPD), lactate dehydrogenases A and B (LDH-A and LDH-B), malic enzyme 2 (ME-2), isocitrate dehydrogenase 1 (ICD-1), phosphogluconate dehydrogenase (PGD), glutamate-oxaloacetate transaminase 1 (GOT-1) phosphoglucomutase 2 (PGM-2), leucine aminopeptidase (LAP), glucosephosphate isomerase (GPI), and esterase 2 (ES-2, from kidney). four of the isozymes show patterns that cannot be interpreted by a simple genetic model: esterases 1 and 4 (ES-1, ES-4, from hemolysate), esterase 3 (ES-3, from plasma), and protein 1 (PT-1). The following pairs of loci are assorting independently: LAP and PGD, LAP and PGM-2, GOT-1 and PGD, GOT-1 and GPD, LAP and GPD, GPD and PGD, GPI and PGD. Data from one test cross mating indicate that GPD and PGM-2 are loosely linked with recombination about 30%. Additional data are needed to confirm this relationship.This study was conducted while the first author was the recipient of an NIH Traineeship. The Departments of Genetics and Zoology provided financial support for the maintenance of the animal colony. This work was supported in part by an NIH-Biomed grant (3-S05-RR-07006-08S1) to W. Z. Lidicker.     

橙腹田鼠中延缓性密度依赖效应和种群波动

检验了延迟的密度依赖对橙腹田鼠 (Microtusochrogaster)一个波动种群的生存和生殖的影响 ,研究持续了 63个月 ,取样间隔为 3 5天。在研究期间 ,该种群的密度经历了 4次波动 ,每次波动的高峰都在 11月至次年 1月 ,种群数量在冬季下降。生存和生殖都有负面的密度依赖效应 ,最大效应具有 2个月的时滞。种群存活率增长对种群密度最大的正面效应具有 2个月的时滞 ,而对与增加生殖则有 3个月的时滞。内部因素和冬季都可能推延对生殖的密度依赖效应 ,但是本文未能检验这些内部因素的影响。季节性影响看来与对生存的延缓性密度依赖效应无关。负面的延缓性密度依赖效应对生存和生殖的净作用可能在于减少、而不是阻止橙腹田鼠种群波动的幅度     

The correlation between demography and metabolic rate: a test using the beach vole (Microtus breweri) and the meadow vole (Microtus pennsylvanicus)

Summary This study examines the hypothesis that mammalian species with wide fluctuations in population size will have greater metabolic rates than species with smaller population fluctuations. We tested this hypothesis using two microtine rodents — the beach vole (Microtus breweri) and the meadow vole (M. pennsylvanicus). Although these species experience similar climatic regimes, eat similar foods, and have a very close phylogenetic relationship, they show marked differences in demography. Microtus pennsylvanicus is prone to large supraannual fluctuations in population size, while M. breweri is essentially acyclical. Metabolic rate (oxygen consumption) of each species was measured using open-flow respirometry at ambient temperatures ranging from 2 to 34° C. Basal metabolic rate of M. pennsylvanicus (1.81 ml O₂ g^–1 h^–1) was significantly greater than that of M. breweri (1.39 ml O₂ g^–1 h^–1). The lower critical temperature, estimated by continuous two-phase regression, was 28.9° C for M. pennsylvanicus and 29.8° C for M. breweri. Regression lines below thermoneutrality did not differ in slope, but the elevation for M. pennsylvanicus was significantly higher. Thus, M. pennsylvanicus has a higher metabolic rate at all temperatures examined. These results support the hypothesis that metabolic rate is positively correlated with the extent of population fluctuation. We suggest that further evidence for, or against, this hypothesis should be found by comparing closely matched species pairs, rather than resorting to confounded allometric comparisons of ecologically and phylogenetically diverse taxa.     

Ongoing ultradian activity rhythms in the common vole,Microtus arvalis,during deprivations of food,water and rest

Summary The timing mechanism underlying ultradian (2–3 h) activity patterns in the common vole, Microtus arvalis, was studied using behavioural deprivation experiments. These were aimed at distinguishing between a homeostatic control mechanism, in which the rhythmic behaviour itself is part of the causal loop, and a clock mechanism, independent of the behaviour.In 175 experiments, deprivation of food during 3 ultradian cycles in (subjective) daytime did not result in significant changes in the ultradian periodicity of attempts to obtain the food, compared with ad lib. access to food and water. A minor, but significant increase in ultradian activity time () occurred in the course of the deprivation, but this was compensated by a shorter ultradian rest (). These results were obtained both in intact animals (n = 24), which showed ultradian and circadian rhythmicity in behaviour, and in animals (n = 21) with electrolytic lesions aimed at the suprachiasmatic nuclei (SCN), which lacked the circadian modulation of behaviour. Simultaneous deprivation of water and food in 8 voles without circadian rhythmicity during 40 experiments also did not lead to any change in the ultradian periodicity of feeding attempts.Rest deprivation was studied in 5 SCN lesioned voles, by forcing running wheel activity to continue following spontaneous running. Thus, the experimental activity bout was artificially lengthened to 2–9 h in 67 experiments. The onset of the subsequent rest episodes occurred independent of the duration of the preceding . The duration of was dependent on the preceding, experimental in a periodic fashion. The interval experimental (=lengthened +following ) was equal to one, two or three times the control (obtained on nonexperimental days). This result fits the prediction of a clock model and is in conflict with a monotonicincrease of with , as expected in a homeostatic, restorative process.It is concluded that the ultradian timing of activity in the common vole can be explained neither by homeostatic hunger or thirst mechanisms nor by homeostatic rest/activity regulation. The results strongly suggest an independent clock system generating ultradian feeding rhythms in the common vole.Abbreviations DD continuous darkness - LD light-dark regime - LL continuous light - RCA retrochiasmatic area - ARC arcuate nucleus - SCN suprachiasmatic nuclei - ultradian period - ultradian activity time - ultradian rest time     

Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences

Voles of the genus Microtus represent one of the most speciose mammalian genera in the Holarctic. We established a molecular phylogeny for Microtus to resolve contentious issues of systematic relationships and evolutionary history in this genus. A total of 81 specimens representing ten Microtus species endemic to Europe as well as eight Eurasian, six Asian and one Holarctic species were sequenced for the entire cytochrome b gene (1140 bp). A further 25 sequences were retrieved from GenBank, providing data on an additional 23, mainly Nearctic, Microtus species. Phylogenetic analysis of these 48 species generated four well-supported monophyletic lineages. The genus Chionomys, snow voles, formed a distinct and well-supported lineage separate from the genus Microtus. The subgenus Microtus formed the strongest supported lineage with two sublineages displaying a close relationship between the arvalis species group (common voles) and the socialis species group (social voles). Monophyly of the Palearctic pitymyid voles, subgenus Terricola, was supported, and this subgenus was also subdivided into two monophyletic species groups. Together, these groupings clarify long-standing taxonomic uncertainties in Microtus. In addition, the "Asian" and the Nearctic lineages reported previously were identified although the latter group was not supported. However, relationships among the main Microtus branches were not resolved, suggesting a rapid and potentially simultaneous radiation of a widespread ancestor early in the history of the genus. This and subsequent radiations discernible in the cytochrome b phylogeny, show the considerable potential of Microtus for analysis of historical and ecological determinants of speciation in small mammals. It is evident that speciation is an ongoing process in the genus and that the molecular data provides a vital insight into current species limits as well as cladogenic events of the past.     

Multi-male mating, probability of conception, and litter size in the prairie vole (Microtus ochrogaster)

We conducted a mating experiment in the laboratory using prairie voles, Microtus ochrogaster, to document that multi-male mating (MMM) can occur in this supposedly monogamous species and to test two hypotheses for the advantages of MMM in female mammals. The two hypotheses are that MMM (1) increases the probability of pregnancy and (2) increases litter size. We also tested the hypothesis that multiple copulations, rather than multiple partners, increases litter size and/or probability of pregnancy. Females were given a choice of mating with any of three males, each of which was tethered in a separate compartment. The mate choice bouts were recorded on videotape. We recorded the number of copulations and number of males with which females mated over a 24 h period. Litter size and probability of pregnancy were not significantly different for females that mated with one, two or three males. Increasing numbers of copulations, independent from the number of males, also did not increase litter size but did significantly increase the probability of pregnancy. MMM, at least in prairie voles, must serve some function other than increasing litter size and probability of conception.     

Progesterone and testosterone concentrations during oestrous cycle and pregnancy in the common vole (Microtus arvalis Pallas)

Serum progesterone and testosterone concentrations were measured during different stages of oestrous and pregnancy in paired and unpaired female common voles (Microtus arvalis). Hormone concentrations were measured by ELISA, and cycle stages were determined by vaginal smears. Paired females usually had serum progesterone concentrations of more than 10 ng/ml in the oestrous cycle. A significant maximum was detected in prooestrous (51.70 +/- 7.84 ng/ml, mean +/- S.D.). Serum progesterone concentrations increased from about 40 ng/ml at the beginning of pregnancy to about 70 ng/ml on days 15 and 16. The last 2 days before parturition (days 19 and 20) were characterised by a decrease of progesterone concentrations to ca. 30 ng/ml. The maximum concentration of testosterone was found in prooestrous (1.58 +/- 0.31 ng/ml). Concentrations during pregnancy varied between 1.5 and 2.1 ng/ml. In two of three cases unpaired females exhibited progesterone values below 10 ng/ml, but with varying vaginal smear patterns. The combination of progesterone concentrations and vaginal smear patterns was found to be regular in only 23.8% of the cases. The most frequent cycle stage found was the oestrous (44.2%). Mean concentrations of progesterone (10.43 +/- 13.81 ng/ml) and testosterone (0.85 +/- 1.11 ng/ml) in unpaired females were significantly lower than in paired females, thereby denoting reproductive inactivity in the former. The study presents basic data for several parameters of the reproductive biology in the common vole and confirms the importance of combining hormone assays and vaginal smear monitoring in reproductive research.     

Summer acclimatization in the short-tailed field vole,Microtus agrestis

We investigated the changes that occurred in basal and noradrenaline-induced metabolic rate, body temperature and body mass in short-tailed field voles,Microtus agrestis, during exposure to naturally increasing photoperiod and ambient temperature. These parameters were first measured in winter-acclimatized voles (n=8) and then in the same voles which had been allowed to seasonally acclimatize to photoperiod and ambient temperature (6 months later). Noradrenaline induced metabolic rate, basal metabolic rate and nonshivering thermogenesis were significantly higher in winter-acclimatized compared to summer-acclimatized voles. There was a significant positive relationship between basal metabolic rate and noradrenaline-induced metabolic rate. Body mass was significantly higher in summer-acclimatized compared to winter-acclimatized voles. There was a significant positive relationship between body mass and noradrenaline-induced metabolic rate in both winter-acclimalized and summer-acclimatized voles; however, there was no relationship between basal metabolic rate and body mass in either seasonal group of voles. Body temperature after measurements of basal metabolic rate was not significantly different in the seasonal cohorts of voles. However, body temperature was significantly higher in winter-acclimatized compared to summer-acclimatized voles after injection of noradrenaline. Previously we have found that a long photoperiod was not a sufficient stimulus to reduce thermogenic capacity in winter-acclimatized voles during cold exposure, since basal metabolic rate increased to compensate for a reduction in regulatory nonshivering thermogenesis. Here we found that a combination of increased ambient temperature and photoperiod did significantly reduce thermogenic capacity in winter-acclimatized voles. This provided evidence that the two aspects of non-shivering thermogenesis, obligatory and regulatory, are stimulated by different exogenous cues. Summer acclimatization in the shorttailed field vole is manifest as a significant decrease in both basal and noradrenaline-induced metabolic rate, combined with a significant increase in body mass.Abbreviations ANCOV A analysis of covariance - BAT brown adipose tissue - BM body mass - BMR basal metabolic rate - NST non-shivering thermogenesis - NA noradrenaline - V the maximum V recorded following mass specific injection of noradrenaline - V the maximum V recorded following mass specific injection of saline - T _a ambient temperature - T _b rectal body temperature - T _1c lower critical temperature - UCP uncoupling protein - V oxygen consumption     

Limits to sustained energy intake IX: a review of hypotheses

Several lines of evidence indicate that animals in the wild may be limited in their maximal rates of energy intake by their intrinsic physiology rather than food availability. Understanding the limits to sustained energy intake is important because this defines an envelope within which animals must trade-off competing activities. In the first part of this review, we consider the initial ideas that propelled this area and experimental evidence connected with them. An early conceptual advance in this field was the idea that energy intake could be centrally limited by aspects of the digestive process, or peripherally limited at the sites of energy utilisation. A model system that has been widely employed to explore these ideas is lactation in small rodents. Initial studies in the late 1980s indicated that energy intake might be centrally limited, but work by Hammond and colleagues in the 1990s suggested that it was more likely that the limits were imposed by capacity of the mammary glands, and other works tended to support this view. This consensus, however, was undermined by studies that showed milk production was higher in mice at low temperatures, suggesting that the capacity of the mammary gland is not a limiting factor. In the second part of the review we consider some additional hypotheses that might explain these conflicting data. These include the heat dissipation limits hypothesis, the seasonal investment hypothesis and the saturated neural control hypothesis. Current evidence with respect to these hypotheses is also reviewed. The limited evidence presently available does not unambiguously support any one of them. Limits to sustained energy intake VIII: Król et al. (2003) J Exp Biol 206:4283-4291.     

A preliminary study of food selection by the orangutan in relation to plant quality

We observed the foraging behavior of orangutans in Central Indonesian Borneo during October, November, and December 1980, and analyzed food and nonfood items for water content, neutral detergent fiber, crude protein, available crude protein, and protein:fiber ratio and the presence of alkaloids and tannins. The diet of the orangutan during this season was unusual because it consisted predominantly of seeds and unripe, rather than ripe, fruits. Also, the major diet item, the seeds ofIrvingia malayana, had been ignored in previous years when it had fruited. In leaves, protein content was more closely associated with food choice than either neutral detergent fiber or the protein:fiber ratio. Flowers had the highest protein content and protein:fiber ratio of any food item. Tannins were found in most food items, but the presence of alkaloids was found in only one.     

Age differences in food intake and dietary selection of wild male Japanese macaques

Age differences in food intake and dietary selection were studied for 8 months among wild male Japanese macaques (Macaca fuscata) under non-predatory situations. Juveniles' feeding time was longer than adult males' in some months, in particular in mating seasons, but did not differ in the other months. Juveniles' feeding speed was slower than that of adult males. However, the age difference in average feeding speed was smaller (90%) than that in expected daily energy expenditure (62–58%). The extent of age difference in feeding speed varied with the food type: the difference was large for fibrous foods, but small for fruits or seeds. As a consequence of the age differences in time spent feeding and feeding speed, the age difference in daily food intake was smaller than expected from metabolic demands. Thus, the hypothesis that juveniles are more vulnerable to starvation than adults was not supported among male Japanese macaques in predator-free Yakushima. Juveniles ate more animal matter, while adult males ate more fibrous foods.     

Microsatellite markers for the common vole (<Emphasis Type="Italic">Microtus arvalis</Emphasis>) and their cross-species utility

Fragmentation of natural habitats of the common vole (Microtus arvalis) provides an excellent model system to study the consequences of restricted gene flow and small population sizes for isolated populations. Here we describe the isolation and characteristics of 10 autosomal and one X-linked microsatellite marker. These new markers were tested in 24 voles from a natural population in eastern Germany. Loci were highly polymorphic with numbers of alleles per locus ranging from three to 26 and expected heterozygosities from 0.51 to 0.97. All loci except for the X-linked locus Mar105 followed Hardy–Weinberg expectations. Cross-species amplifications revealed that most loci were polymorphic as well in M. agrestis, M. thomasi, and M. pennsylvanicus.     

高纤维食物对黄毛鼠摄食和消化的影响

动物的消化生理特征和消化对策可决定其营养生态位。为揭示黄毛鼠适应高纤维食物的消化对策,在高纤维食物饲喂10 d和20 d时,以食物平衡法测定摄食量、粪便量及相应的能量学参数。在取食高纤维食物10 d时,摄食量无显著变化,但粪便量显著增加,消化率显著下降;至20 d时,摄食量显著增加,消化率仍低于对照组,但消化能与对照组无差异。高纤维组动物的体重在第10 d时显著下降,但在第20 d时未进一步下降。该结果表明,黄毛鼠能够通过增加摄食量和降低消化率的消化对策适应高纤维食物,此外,降低体重使总能量需求减少,也是其适应低质量食物的对策之一。     

Demography of a mediterranean microtine: the Mediterranean pine vole,Microtus duodecimcostatus

Microtus duodecimcostatus in a mediterranean vole which is not known to display spectacular increases in population numbers as in some microtine species. A population was studied in southern France with a capture-recapture method. The population included resident adults which have a high and constant survival rate (monthly estimate: 0.879), erratic adults (those caught once only), and juveniles which have a lower and constant survival rate. The adult survival rate was not sexbiased but the juvenile survival rate was higher in males (monthly estimates: 0.710 and 0.596 for males and females, respectively). Adult body weight did not vary seasonally. Residents had a higher mean body weight than erratics. Reproduction occurred all the year round. The proportion of reproductive females was higher among residents than among erratics. Population numbers varied seasonally. Our study points out thatM. duodecimcostatus is very different from microtine species which display cyclic fluctuations. Population studies on the subgenusPitymys (which containsM. duodecimcostatus and its closest related species) suggest that they are typically non-cyclic. The importance of social factors in the control of reproduction and maturation was evidenced inM. pinetorum. The role of such factors in the population regulation ofM. duodecimcostatus is discussed.     

Patterns of resource use,food quality,and health status of voles (Microtus pennsylvanicus) trapped from fluctuating populations

Summary Recent studies suggest that diet quality is responsible for differential survivorship of vole cohorts (Boonstra and Boag 1987) and spacing behavior of females (Ims 1987). These phenomena have been related either to a lack of or a deterioration in the quality of the preferred food. To test this hypothesis, we compared foods habits, food quality and health status of meadow voles (Microtus pennsylvanicus) from high and low population density phases. In this study, seven plant species represented the main food items used on a regular basis and biomass values of preferred species decreased with browsing pressure. In addition, food quality of the main dietary items changed between phases forcing females to adjust their feeding strategy accordingly. Health of voles changed also opening the way to speculations on competition for high quality food resources and survivorship.     

Meadow voles and prairie voles differ in the percentage of conspecific marks they over-mark

Many terrestrial mammals scent mark in areas containing the scent marks of conspecifics, and thus, may deposit their own scent marks on top of those that were deposited previously by conspecifics. This phenomenon, known as over-marking appears to play a role in same-sex competition or mate attraction. The present study determines whether meadow and prairie voles avoid over-marking the scent marks of conspecifics, target the scent marks of conspecifics and over-mark them, or randomly over-mark the scent marks of conspecifics. The data show that meadow and prairie voles adjust the number and location of scent marks that they deposit in areas marked previously by particular conspecifics. Male and female meadow and prairie voles target the scent marks of opposite-sex conspecifics and over-mark them. Female meadow and prairie voles also target the scent marks of female conspecifics. In contrast, male meadow and prairie voles over-mark the scent marks of male conspecifics in a random manner. By differentially over-marking the scent marks of conspecifics, voles may be able to communicate particular information to a variety of conspecifics.     

Age variation in a fluctuating population of the common vole

We analysed variation in age in a fluctuating population of the common vole (Microtus arvalis) in southern Moravia, Czech Republic, to test the assumption of the senescence hypothesis that the age of voles increases with increasing population density. Between 1996 and 1998, we monitored the demographic changes by snap-trapping and live-trapping in a field population passing through the increase, peak and decline phase of the population cycle. We used the eye lens mass method to determine the age of snap-trapped animals and those that died in live-traps. The average age of winter males was clearly higher after the peak phase breeding season than before it. No such phase-dependent shift in age, however, was observed in the female component. Male age continued to increase from autumn to spring over the pre-peak winter, and the highest age was in spring of the peak phase year. However, after the peak phase breeding season the highest age was achieved in winter, with the decline phase males during the next spring tending to be younger. The average age of females in spring populations was always lower than in winter populations. The average age of voles from live-traps was always higher than voles from snap-traps, particularly in winter and spring populations, suggesting the presence of senescent animals. Although the density-dependent changes in age are consistent with those observed for other voles, they provide only weak evidence that population cycles in the common vole are accompanied by pronounced shifts in individual age, particularly in female voles.Due to an error in the citation line, this revised PDF (published in December 2003) deviates from the printed version, and is the correct and authoritative version of the paper.     

Vegetation analysis in colonies of an endangered rodent, the Cabrera vole (Microtus cabrerae), in southern Portugal

The Cabrera vole (Microtus cabrerae) is a threatened rodent endemic in the Iberian Peninsula with a patchy distribution and specific microhabitat requirements. This aim of this study was to document the composition of plant communities in habitats of Cabrera vole colonies in southern Portugal. Differences observed in plant species composition were also compared with vegetation structure, taxonomic and life form groups, species and group diversity, disturbance, topography and soil properties. Vegetation was sampled between March and July 2004, in 26 colonies occurring in five geographical areas. Grasses were the most abundant, common and diverse family in the colonies, and the perennial grass Agrostis castellana was present in 92% of colonies, with a mean cover of 16% of the site. Other frequently occurring species were Briza maxima (85%), Vulpia myuros (85%), Gaudinia fragilis (81%), Leontodon spp. (81%), Avena barbata (77%), Bromus hordeaceus (77%) and Tolpis barbata (77%). Colonies were classified in eight vegetation groups that included meadows, tall perennial grasslands, manured meadows with tall sedges, annual grasslands and ruderal and nitrophilous grasslands. Main gradients associated with composition differences were grass richness, annual and perennial grass cover, vegetation structure (herbaceous vegetation height), soil properties (texture and moisture), disturbance (ruderal species) and colony dimensions (area). Results suggest that the Cabrera vole is able to exploit a wide variety of grasslands, with a varying degree of ecological disturbance. Meadows and perennial grassland communities seem to be higher-quality microhabitats for voles.     

Food deprivation in the common vole (<Emphasis Type="Italic">Microtus arvalis</Emphasis>) and the tundra vole (<Emphasis Type="Italic">Microtus oeconomus</Emphasis>)

Arvicolinae voles are small herbivores relying on constant food availability with weak adaptations to tolerate prolonged food deprivation. The present study performed a comparative analysis on the responses to 4–18 h of food deprivation in the common vole (Microtus arvalis) and the tundra vole (Microtus oeconomus). Both species exhibited rapid decreases in the plasma and liver carbohydrate concentrations during phase I of fasting and the decline in the liver glycogen level was more pronounced in the tundra vole. The plasma thyroxine concentrations of the common vole decreased after 4 h. Lipid mobilization (phase II of fasting) was indicated by the increased plasma free fatty acid levels after 8–18 (the common vole) or 4–18 h (the tundra vole) and by the elevated lipase activities. In the tundra vole, the plasma ghrelin concentrations increased after 12 h possibly to stimulate appetite. Both species showed increased liver lipid concentrations after 4 h and plasma aminotransferase and creatine kinase activities after 12–18 h of food deprivation implying liver dysfunction and skeletal muscle damage. No signs of stimulated protein catabolism characteristic to phase III of fasting were present during 18 h without food.