Effects of anesthetics on cardiovascular responses of the marmot Marmota flaviventris

The effects of pentobarbital (30 mg/kg), urethan (2 g/kg), chloralose/urethan (50 mg/kg, 500 mg/kg), and thiobutabarbital (Inactin, 100 mg/kg) on the mean arterial pressure (BP) and heart period (HP) of Marmota flaviventris were examined. Anesthesia significantly decreased BP by 22-27 mm Hg and HP by 123-151 msec. In a series of paired studies with eight marmots it was found that pentobarbital increased the BP response to phenylephrine and almost abolished the baroreflex HP responses to phenylephrine and nitroglycerin. In another series of animals right carotid occlusion in unanesthetized animals produced greater changes in BP and HP than occlusion of the left carotid. Chloralose/urethan, urethan, or Inactin reduced the reflex BP response to unilateral carotid occlusion by 50% and the HP response by 96%. It was concluded that the anesthetic agents investigated depress baroreflex responses significantly by influencing efferent sympathetic and parasympathetic reflex responses. They, therefore, are not appropriate for cardiovascular studies in acute, anesthetized preparations of the marmot and, perhaps, other hibernating species.     

Caching behaviour by eastern woodrats,Neotoma floridana,in relation to food perishability

Two experiments were conducted on eastern woodrats to determine whether the preference for food items gathered for their caches and the sequence of use of items in the cache varied with perishability. In the first experiment, woodrats were given either 2 kg each of two non-perishable items, laboratory chow and bur oak acorns (which they used more than chow), or 2 kg each of preferred, but perishable, grapes and the non-perishable chow. As hypothesized, the woodrats both ate and stored acorns when they were paired with chow (there would be no advantage to either eating or storing the less-used chow). In contrast, when given grapes and chow, the woodrats continued to eat grapes but stored primarily chow. That is, the utility of the items appeared to change depending on whether they were to be eaten or stored. In the second experiment, woodrats were given excess amounts of chow or grapes that were 2, 4, 6 and 8 days old. They ingested chow in the proportions available, as the chow did not spoil with age. However, the consumed grapes in proportions significantly different from those available. It was anticipated that they would eat the oldes grapes first and store the freshest grapes, but neither this pattern nor any other was obvious in ralation to the age of the grapes. The results suggest that woodrats discriminate between food items based on their perishability, and vary their decisions about what to ingest and store accordingly.     

Comparison of surface temperature in 13-lined ground squirrel (Spermophilus tridecimlineatus) and yellow-bellied marmot (Marmota flaviventris) during arousal from hibernation

Surface temperatures (Ts) of eight 13-lined ground squirrels and seven yellow-bellied marmots were measured during arousal from hibernation using infrared thermography (IRT) and recorded on videotape. Animals aroused normally in 5 degrees C cold rooms. Body temperatures were recorded during arousal using both cheek pouch and interscapular temperature probes. Warming rate in arousal was exponential. Mean mass specific warming rates show the squirrels warm faster (69.76 degrees C/h/kg) than the marmots (4.49 degrees C/h/kg). Surface temperatures (Ts) for 11 regions were measured every few minutes during arousal. The smaller ground squirrel shows the ability to perfuse distal regions without compromising rise in deep body temperature (Tb). All squirrel Ts's remained low as Tb rose to 18 degrees C, at which point, eyes opened, squirrels became more active and all Ts's rose parallel to Tb. Marmot Ts remained low as Tb rose initially. Each marmot showed a plateau phase where Tb remained constant (mean Tb 20.3+/-1.0 degrees C, duration 9.4+/-4.1 min) during which time all Ts's rose, and then remained relatively constant as Tb again began to rise. An anterior to posterior Ts gradient was evident in the ground squirrel, both body and feet. This gradient was only evident in the feet of the marmots.     

Evaluation of three combinations of anesthetics for use in free-ranging alpine marmots (Marmota marmota)

From April 1998 to September 2000, 241 free-ranging alpine marmots (Marmota marmota) were anesthetized in the course of a field project using either xylazine plus ketamine (XK), medetomidine plus ketamine (MK), or xylazine plus a 1:1 mixture of zolazepam and tiletamine (XZT). For each of the combinations, the respective doses for short term and long-term surgery were established and seasonal variations in the amount of drugs needed were assessed. No fatalities occurred, and doses for efficient and safe anesthesia in spring were as follows (XK, MK, and XZT, respectively, in mg/kg body mass): short term surgery 3 + 40, 0.25 + 35, and 3 + 15; long term surgery 20 + 80, 0.5 + 70, and 10 + 20. In late summer/autumn, higher doses (20 + 60, 0.2 + 60, and 10 + 15 for short term surgery) had to be administered, probably due to increase of marmots' body fat content. Heart rate, respiratory rate, rectal temperature, palpebral reflex, muscle relaxation, and analgesia were monitored to evaluate the animals' responses to each of the drug combinations. Hypothermia was induced by all combinations and heart rate significantly decreased during anesthesia, especially in marmots receiving MK. Respiratory rate was highly variable and no significant differences between the drugs were found. Muscle relaxation was rather poor in marmots anesthetized with XK. The XZT combination tended to have a longer induction period but was found to subsequently depress the palpebral reflex and induce muscle relaxation and analgesia very efficiently. We conclude that, regardless of the anesthetics used, doses should always be adjusted to the planned manipulations, the marmots' nutritional state, and to the time of year. Furthermore, close monitoring of physiologic parameters, especially body temperature, should be guaranteed. On the basis of physiologic and behavioral responses, XZT is the most effective drug combination for anesthetizing alpine marmots, especially for long term, potentially painful procedures.     

Anesthesia of marmots with sodium pentobarbital, ketamine hydrochloride, and a combination of droperidol and fentanyl.

Three different anesthetics were tried on wild marmots to immobilize them sufficiently for intra-oral physiologic measurements and dental examination. Essentially the same procedure was performed or attempted on 15 animals. The droperidol (20 mg/ml) and fentanyl (0.4 mg/ml) combination gave better results than sodium pentobarbital or ketamine hydrochloride and was therefore used in most instances. We concluded that the dose rate should be adjusted to the nutritional state of the animal as well as to the absolute weight.     

Epizootiology of arenaviral infections in the white-throated woodrat (Muridae: Sigmodontinae) and other woodrats in Arizona.

The purpose of this study was to extend and refine our knowledge of the geographical distribution and natural host relationships of the arenaviruses associated with woodrats indigenous to Arizona. Antibody to a Tacaribe serocomplex virus was found in 112 of 1,250 white-throated woodrats, five of 208 Mexican woodrats, one of 114 Stephen's woodrats, and none of 862 other rodents captured at 51 sites in 10 counties in Arizona. Of the 112 antibody-positive white-throated woodrats, 109 (97.3%) were captured within extensive, dense patches of prickly pear cactus and cane cholla in three counties in mid-central Arizona. Analysis of the serological and zoographical data suggested that white-throated woodrats usually become infected early in life and that the distribution of antibody-positive white-throated woodrats in Arizona is not linked to a specific biome.     

Regulation of body temperature and energy requirements of hibernating alpine marmots (Marmota marmota)

Body temperature and metabolic rate were recorded continuously in two groups of marmots either exposed to seasonally decreasing ambient temperature (15 to 0 degrees C) over the entire hibernation season or to short-duration temperature changes during midwinter. Hibernation bouts were characterized by an initial 95% reduction of metabolic rate facilitating the drop in body temperature and by rhythmic fluctuations during continued hibernation. During midwinter, we observed a constant minimal metabolic rate of 13.6 ml O(2) x kg(-1) x h(-1) between 5 and 15 degrees C ambient temperature, although body temperature increased from 7.8 to 17.6 degrees C, and a proportional increase of metabolic rate below 5 degrees C ambient temperature. This apparent lack of a Q(10) effect shows that energy expenditure is actively downregulated and controlled at a minimum level despite changes in body temperature. However, thermal conductance stayed minimal (7.65 +/- 1.95 ml O(2) x kg(-1) x h(-1) x degrees C(-1)) at all temperatures, thus slowing down cooling velocity when entering hibernation. Basal metabolic rate of summer-active marmots was double that of winter-fasting marmots (370 vs. 190 ml O(2) x kg(-1) x h(-1)). In summary, we provide strong evidence that hibernation is not only a voluntary but a well-regulated strategy to counter food shortage and increased energy demands during winter.     

Comparison of blood leptin and vitamin E and blood and adipose fatty acid compositions in wild and captive populations of critically endangered Vancouver Island marmots (Marmota vancouverensis)

Vancouver Island marmots (Marmota vancouverensis) (VIMs) are a critically endangered species of fat-storing hibernators, endemic to Vancouver Island, British Columbia, Canada. In addition to in-situ conservation efforts, a captive breeding program has been ongoing since 1997. The captive diet is mostly pellet-based and rich in n−6 polyunsaturated fatty acids (PUFAs). In captivity, overall length of hibernation is shortened, and marmots have higher adipose tissue reserves compared to their wild-born counterparts, which may be a risk factor for cardiovascular disease, the leading cause of mortality in captive marmots. To investigate differences in lipid metabolism between wild and captive populations of VIMs, blood vitamin E, fatty acid (FA) profiles and leptin, and white adipose tissue (WAT) FA profiles were compared during the active season (May to September 2019). Gas chromatography, high-performance liquid chromatography, and multiplex kits were used to obtain FA profiles, α-tocopherol, and leptin values, respectively. In both plasma and WAT, the concentration of the sum of all FA in the total lipids was significantly increased in captive VIMs. The n−6/n−3 ratio, saturated FAs, and n−6 PUFAS were higher in captive marmots, whereas n−3 PUFAs and the HUFA score were higher in wild marmots. Serum concentrations of α-tocopherol were greater by an average of 45% in captive marmots, whereas leptin concentrations did not differ. Results from this study may be applied to improve the diet and implement weight management to possibly enhance the quality of hibernation and decrease the risk of cardiovascular and metabolic diseases of captive VIMs.     

Ectoparasites,Fitness, and Social Behaviour of Yellow-Bellied Marmots

Parasites can cause a loss of fitness for their hosts, potentially influencing social behaviour patterns of the host that promote or hinder parasite transmission. I studied yellow-bellied marmots (Marmota flaviventris) and their ectoparasites to determine if ectoparasites reduce the fitness of marmots and to test whether ectoparasite loads differ according to social behaviour. Three taxa of ectoparasites were identified, fleas (Oropsylla Stanfordi), lice (Linognathoides marmotae), and mites (family Dermanyssidae). High ectoparasite loads were related to slower growth, lower overwinter survival, and reduced reproduction, suggesting that ectoparasites are a fitness cost for marmots. Ectoparasite loads were not higher in colonial than in noncolonial marmots, nor in polygynous than in monogamous adult males. There was a trend, however, toward higher ectoparasite loads in marmots that were dispersing rather than philopatric. Further, ectoparasite loads differed among groups of marmots that nested or hibernated communally, indicating that spatial scale is important in understanding the relationships between parasites and social behaviour.     

Ambient temperature influences diet selection and physiology of an herbivorous mammal, Neotoma albigula

The whitethroat woodrat (Neotoma albigula) eats juniper (Juniperus monosperma), but the amount of juniper in its diet varies seasonally. We tested whether changes in juniper consumption are due to changes in ambient temperature and what the physiological consequences of consuming plant secondary compounds (PSCs) at different ambient temperatures might be. Woodrats were acclimated to either 20 degrees C or 28 degrees C. Later, they were given two diets to choose from (50% juniper and a nontoxic control) for 7 d. Food intake, resting metabolic rate (RMR), and body temperature (T(b)) were measured over the last 2 d. Woodrats at 28 degrees C ate significantly less juniper, both proportionally and absolutely, than woodrats at 20 degrees C. RMRs were higher for woodrats consuming juniper regardless of ambient temperature, and T(b) was higher for woodrats consuming juniper at 28 degrees C than for woodrats eating control diet at 28 degrees C. Thus, juniper consumption by N. albigula is influenced by ambient temperature. We conclude that juniper may influence thermoregulation in N. albigula in ways that are helpful at low temperatures but harmful at warmer temperatures in that juniper PSCs may be more toxic at warmer temperatures. The results suggest that increases in ambient temperature associated with climate change could significantly influence foraging behavior of mammalian herbivores.     

Evidence for local specialization in a generalist mammalian herbivore, Neotoma fuscipes

Herbivores with very plastic dietary requirements, or so-called generalist species, can include individuals that develop specialized feeding habits through their experience with local chemically-defended plants. Local specialization has important implications for understanding a variety of ecological and evolutionary dynamics. However, the extent to which individuals within a generalist species specialize on local plants and the consequences of such specialization remain poorly understood, especially in non-insect herbivores. To better understand this phenomenon, we determined the diet and food preferences of a generalist mammalian herbivore, the dusky-footed woodrat ( Neotoma fuscipes ), in two adjacent but distinct plant communities. Based on a combination of cafeteria trials and stable isotope analyses (δ¹³C and δ¹⁵N), our results indicate that woodrats display preferences for local plants and tend to avoid novel chemically-defended plants. Moreover, both methodologies support the conclusion that individual woodrats are dietary specialists restricting their diets to only a few (2-3) of the available plant species. In juniper woodland, woodrats prefer western juniper ( Juniperus occidentalis ), while less than one km away in mixed-coniferous forest, woodrats prefer incense cedar ( Calocedrus decurrens ). Both plants contain high levels of plant secondary compounds that require detoxification mechanisms within consumers. Therefore, preferences are likely indicative of underlying physiological adaptations that could promote further behavioral, physiological and ultimately genetic differences between woodrats in different habitats. This study provides additional evidence for local specialization and urges caution when using the term generalist to characterize feeding behaviors at the individual level.     

Comparison of discriminant function and classification tree analyses for age classification of marmots

We evaluated the predictive power of two classification techniques, one parametric – discriminant function analysis (DFA) and the other non-parametric – classification and regression tree analysis (CART), in order to provide a non-subjective quantitative method of determining age class in Vancouver Island marmots ( Marmota vancouverensis ) and hoary marmots ( Marmota caligata ). For both techniques we used morphological measurements of known-age male and female marmots from two independent population studies to build and test predictive models of age class. Both techniques had high predictive power (69–86%) for both sexes and both species. Overall, the two methods performed identically with 81% correct classification. DFA was marginally better at discriminating among older more challenging age classes compared to CART. However, in our test samples, cases with missing values in any of the discriminant variables were deleted and hence unclassified by DFA, whereas CART used values from closely correlated variables to substitute for the missing values. Therefore, overall, CART performed better (CART 81% vs DFA 76%) because of its ability to classify incomplete cases. Correct classification rates were approximately 10% higher for hoary marmots than for Vancouver Island marmots, a result that could be attributed to different sets of morphological measurements. Zygomatic arch breadth measured in hoary marmots was the most important predictor of age class in both sexes using both classification techniques. We recommend that CART analysis be performed on data-sets with incomplete records and used as a variable screening tool prior to DFA on more complete data-sets.     

Isolation and characterization of microsatellite markers in hoary marmots (Marmota caligata)

Microsatellite loci were developed from hoary marmots (Marmota caligata) to aid in the investigation of the social structure and mating system of this species. Seven of the microsatellite loci developed were found to be moderately polymorphic with between two and seven alleles per locus. In addition to the microsatellites developed in hoary marmots we also tested markers developed for other scuirids, namely European alpine marmots (M. marmota), Columbian ground squirrels (Spermophilus columbianus) and European ground squirrels (S. citellus). Of these markers, 13 were polymorphic when amplified in hoary marmots with between two and nine alleles per locus.     

Seasonal glucose uptake in marmots (Marmota flaviventris): the role of pancreatic hormones.

1. Glucose uptake was measured throughout the year in marmots (Marmota flaviventris) by the hyperglycemic clamp technique. During each 2 hr experiment, the plasma glucose level was maintained at 215 mg/dl while blood samples were collected and analysed for glucose, insulin, glucagon, cortisol and catecholamines. 2. Glucose uptake was calculated from the glucose infusion rate, changes in the glucose pool (using a correction factor), and urinary glucose excretion. 3. In autumn, animals peaked in body weight (greater than 4.0 kg) and ceased to feed. Basal plasma insulin levels in autumn were significantly elevated over all other seasons (P less than 0.01) and glucose uptake in autumn was 9.7 +/- 2.4 mg/min which was significantly lower (P less than 0.05) than summer (21.7 +/- 2.4 mg/min) during the steady state phase of the glucose clamp (90-120 min). 4. Plasma glucagon levels declined during the clamp in all seasons but there was no significant difference between seasons. Plasma cortisol and catecholamine (norepinephrine and epinephrine) levels remained unchanged under basal and experimental conditions throughout the seasons. 5. During glucose infusion, beta-hydroxybutyrate levels were suppressed suggesting that lipolysis was reduced during the experiment. 6. These results suggest that the marmot exhibits seasonal changes in glucose uptake; the lowest rate of glucose uptake occurring in the autumn after the animals peak in body weight and cease to feed.     

Description and epidemiology of Theileria youngi n. sp. from a northern Californian dusky-footed woodrat (Neotoma Fuscipes) population

An epidemiologic study designed to identify the small mammal reservoir for the zoonotic WA1-type babesial parasite resulted in the discovery of a small, intraerythrocytic piroplasm in smeared blood from dusky-footed woodrats (Neotoma fuscipes) in northern California. The woodrat parasites were isolated and compared to other piroplasm parasites based on their morphology, antigenicity, and genetic characteristics. These studies indicated that the woodrat parasites were not the WA1-type babesial agent but were of the genus Theileria. We accordingly named it Theileria youngi. The prevalence in the woodrat population was high (61%). Infection was unrelated to gender or age of the woodrats. Potential vectors for this tick-transmitted parasite included 3 species of ticks recovered from the woodrats. Dermacentor occidentalis, Ixodes woodi, and Ixodes pacificus. Mostly larval or nymphal stages were recovered, suggesting transstadial transmission is possible. This is the first piroplasm fully characterized from a dusky-footed woodrat.     

Expression of biotransformation genes in woodrat (Neotoma) herbivores on novel and ancestral diets: identification of candidate genes responsible for dietary shifts

The ability of herbivores to switch diets is thought to be governed by biotransformation enzymes. To identify potential biotransformation enzymes, we conducted a large-scale study on the expression of biotransformation enzymes in herbivorous woodrats ( Neotoma lepida ). We compared gene expression in a woodrat population from the Great Basin that feeds on the ancestral diet of juniper to one from the Mojave Desert that putatively switched from feeding on juniper to feeding on creosote. Juniper and creosote have notable differences in secondary chemistry, and thus, should require different biotransformation enzymes for detoxification. Individuals from each population were fed juniper and creosote diets separately. After the feeding trials, hepatic mRNA was extracted and hybridized to laboratory rat microarrays. Hybridization of woodrat samples to biotransformation probes on the array was 87%, resulting in a total of 224 biotransformation genes that met quality control standards. Overall, we found large differences in expression of biotransformation genes when woodrats were fed juniper vs. creosote. Mojave woodrats had greater expression of 10× as many biotransformation genes as did Great Basin woodrats on a creosote diet. We identified 24 candidate genes that may be critical in the biotransformation of creosote toxins. Superoxide dismutase, a free radical scavenger, was also expressed to a greater extent by the Mojave woodrats and may be important in controlling oxidative damage during biotransformation. The results are consistent with the hypothesis that biotransformation enzymes limit diet switching and that woodrats in the Mojave have evolved a unique strategy for the biotransformation of creosote toxins.     

Pancreatic A and B cell stimulation in euthermic and hibernating marmots (Marmota flaviventris): effects of glucose and arginine administration

Summary In euthermic and hibernating marmots (Marmota flaviventris), the pancreatic A and B cells respond in the appropriate secretory manner to glucose or arginine injection. Although reduced, this response, is clearly present in hibernating marmots. When glucose is administered to euthermic or hibernating marmots, plasma insulin concentrations rise and glucagon levels fall. While similar results are obtained in hibernation, the time period of the response is much longer due to the slowing of temperature dependent metabolic processes. Injection ofl-arginine stimulates an increase in plasma glucose, insulin, and glucagon as expected. Measurements of plasma glucose, insulin, and glucagon under basal conditions, suggest that there are no significant differences between any phase of hibernation (eg. entrance, deep hibernation, arousal) and euthermia. These results provide indirect evidence that the pancreatic A and B cells of hibernating marmots continue to function in order to help regulate plasma glucose concentration.     

Predator discrimination and 'personality' in captive Vancouver Island marmots (Marmota vancouverensis)

A major impediment to recovering declining populations successfully is the mortality of reintroduced or translocated animals. We generally assume that captive-born animals may lose their antipredator behaviour abilities in captivity, but studies rarely compare predator recognition abilities of captive-born and wild-captured animals to test this. To identify whether predator discrimination abilities of the critically endangered Vancouver Island marmots Marmota vancouverensis were lost in captivity, we presented wild-captured and captive-born marmots with taxidermic mounts of predators (a cougar Felis concolor and wolf Canis lupus ) together with control stimuli (marmot, domestic goat Capra aegagrus , the cart on which all stimuli were presented and a 'blank' no-stimulus control). Regardless of specific predator discrimination abilities, for some species overall 'personality' may be associated with response to predators and subsequent survival. Thus, to quantify overall reactivity in the presence of a predator, we also conducted a mirror-image stimulus (MIS) presentation experiment where marmots were video-recorded with or without the presence of a wolf. Marmots discriminated among these stimuli, responding the most to the wolf and cougar. The MIS results suggest that marmots varied along a continuum of reactivity. The amount of reactivity was unaffected by the presence of a wolf, and was correlated with our highest level of responsiveness (vigilance at the burrow and time within the burrow) to the wolf. Taken together, we conclude that marmots differentiate predators from non-predators and that this ability has not been lost under the conditions in which they have been reared.     

Plant secondary metabolites alter the feeding patterns of a mammalian herbivore (<Emphasis Type="Italic">Neotoma lepida</Emphasis>)

Mammalian herbivores are predicted to regulate concentrations of ingested plant secondary metabolites (PSMs) in the blood by modifying the size and frequency of feeding bouts. It is theorized that meal size is limited by a maximum tolerable concentration of PSMs in the blood, such that meal size is predicted to decrease as PSM concentration increases. We investigated the relationship between PSM concentration in the diet and feeding patterns in the herbivorous desert woodrat (Neotoma lepida) fed diets containing phenolic resin extracted from creosote bush (Larrea tridentata). Total daily intake, meal size and feeding frequency were quantified by observing the foraging behavior of woodrats on diets containing increasing concentrations of creosote resin. Desert woodrats reduced meal size as resin concentration in the diet increased, resulting in an overall reduction in daily intake and regulation of resin intake. Moreover, desert woodrats were able to detect resin concentrations in the diet and regulate the intake of resin very rapidly. We suggest that the immediate and sustained ability to detect and regulate the intake of resin concentrations during each foraging bout provides a behavioral mechanism to regulate blood concentrations of resin and allows desert woodrats to make “wise” foraging decisions.     

Locomotor Ability and Wariness in Yellow-Bellied Marmots

Animals employ a variety of behaviors to reduce or manage predation risk. Often, these are studied in isolation, but selection may act on packages of behavior that are referred to as behavioral syndromes. We focused on yellow‐bellied marmots (Marmota flaviventris) and examined three commonly studied antipredator behaviors. We fitted general linear models to explain variation in maximum running speed, time allocated to vigilance and foraging during bouts of foraging, and flight initiation distance (FID). Marmot maximum running speed was influenced by the substrate run across; marmots ran fastest across dirt or low vegetation and slowest across stones or talus. Incline and several other variables shown to affect running speed in other marmot species failed to explain significant variation in yellow‐bellied marmots. From these results we expected marmots to be sensitive to substrate while foraging, but insensitive to incline. However, time allocated to foraging was affected by incline but not by substrate. In bouts of foraging observed in different habitats, and on different inclines, more time was allocated to foraging and less to vigilance on steep slopes and less on level ground. Substrate influenced FID. Marmots in tall vegetation were less tolerant of an approaching person than were those in shorter vegetation. Finally, we found significant correlations between the residuals from the maximum running speed model and the residuals from the time allocated to vigilance and foraging models. We found a tendency for marmots that ran slower than predicted to be less vigilant while foraging. We also found that relatively slow marmots engaged in more active foraging and less vigilance during foraging bouts. This finding suggests a ‘locomotor ability‐wariness while foraging’ syndrome. It also suggests that vulnerable individuals minimize their exposure while foraging.