Optimal Body Size and Energy Expenditure during Winter: Why Are Voles Smaller in Declining Populations? (original) (raw)
Related papers
Journal of Animal ecology, 2001
Over-winter mortality in small mammals is influenced strongly by low ambient temperatures. Individuals with greater thermogenic capacities might then be expected to survive better than those with lower thermogenic capacities. 2. To test this hypothesis, short-tailed field voles Microtus agrestis (Linnaeus) were captured during the winters of 1995/96 and 1996/97 at two field sites near Aberdeen (57 ° N). The captured animals were tagged and taken back to the laboratory, where their resting metabolism (RMR), thermogenic capacity (NA induced metabolism excluding RMR) and body mass were measured. 3. Body mass, RMR and thermogenic capacity did not differ significantly between the start and end of winter in voles that were captured at both times. 4. Body mass varied significantly over the winter months, being lowest in January and highest in March. Thermogenic capacity also varied over the winter and the variation was linked significantly with changes in ambient temperature, suggesting that either voles with greater thermogenic capacity were more likely to be active on cold nights, or voles were flexible in their thermogenic capacities. RMR did not vary significantly over the winter. 5. Animals that survived the winter had a significantly higher residual RMR than those that died (or permanently emigrated) but the survivors did not have significantly greater body masses, RMRs, thermogenic capacities or residual thermogenic capacities.
Global Change Biology, 2016
The cumulative effects of climate warming on herbivore vital rates and population dynamics are hard to predict, given that the expected effects differ between seasons. In the Arctic, warmer summers enhance plant growth which should lead to heavier and more fertile individuals in the autumn. Conversely, warm spells in winter with rainfall (rain‐on‐snow) can cause ‘icing’, restricting access to forage, resulting in starvation, lower survival and fecundity. As body condition is a ‘barometer’ of energy demands relative to energy intake, we explored the causes and consequences of variation in body mass of wild female Svalbard reindeer (Rangifer tarandus platyrhynchus) from 1994 to 2015, a period of marked climate warming. Late winter (April) body mass explained 88% of the between‐year variation in population growth rate, because it strongly influenced reproductive loss, and hence subsequent fecundity (92%), as well as survival (94%) and recruitment (93%). Autumn (October) body mass affec...
The association between body mass, metabolic rates and survival of bank voles
Functional Ecology, 2009
Many studies have been performed in an attempt to explain physiological, ecological and evolutionary factors behind inter-and intraspecific variation in basal metabolic rate (BMR) and maximum aerobic metabolic rate (VO 2max ). However, very little is known about the association between the traits and fitness components in populations of free-living animals. 2. We studied the association between body size and the metabolic rates of bank voles Myodes ( = Clethrionomys ) glareolus and their survival, measured by repeated trappings across 2 years in an isolated, island population. All measured traits (body mass, BM; head width, HW; VO 2max and BMR) were significantly repeatable over short (mean 5·4 days) and long (mean 56·4 days) intervals. 3. Logistic regression analyses showed no consistent relationship between the measured traits and survival until the next trapping session. The correlations, if present, differed in direction between sessions and sexes. Survival over winters was negatively correlated with BM in males ( P = 0·001) but not in females ( P = 0·43). The logistic regression with quadratic effects revealed stabilizing selection on VO 2max in males (across all sessions: P = 0·010; in breeding seasons only: P = 0·001). 4. Both the presence of stabilizing selection and the opposite direction of the selection between sexes and/or seasons could contribute to the relatively high additive genetic variance of metabolic rates, reported earlier in the bank voles.
Ecology, 2013
The interplay between density and climate in shaping the dynamics of herbivore populations is widely acknowledged, and current research is fueled by the identification of mechanisms underlying their effects on individuals and populations. We assessed whether forage availability mediated the effects of density and winter climate on body mass of whitetailed deer (Odocoileus virginianus) yearlings by experimentally reducing deer density to 7.5 and 15 deer/km 2 during eight growing seasons, and by using causal (graphical) hierarchical models and Bayesian hierarchical modeling to assess relationships. The abundance of preferred forage decreased with deer density and varied quadratically (positive parabola) with winter North Atlantic Oscillation (NAO), whereas the fall mass of yearlings increased with forage abundance and spring mass. Fall mass did not differ between experimentally reduced deer densities, yet experimental yearlings were 30% heavier than yearlings harvested at ambient densities. Hence, forage abundance simultaneously mediated the effects of density and climate on fall body mass, which was also influenced by carry-over effects of spring body mass. Our findings increase our ability to anticipate how temperate large herbivores will respond to ongoing changes in intrinsic (e.g., large-herbivore density) and extrinsic (e.g., climate) factors.
Energetics and the evolution of body size in small terrestrial mammals.
Symposia of the Zoological Society of London, 1995
Many species of very small terrestrial mammals exhibit dinal patterns in their body size, ofren with larger individuals predominating in populations from higher latitudes (Berg mann's law). Classically, this pattern has been explained as reflecting the advantageous surface-to-volume ratio of larger animals, which provides them with a thermoregulatory advantage in colder regions, because it reduces their energy demands. Attempts to expand on this energetics explanation are, however, fraught with difficulty. A major problem relates to the fact that it is not possible to speculate on the direction of selection on body size by considering costs alone. However, when both costs and gains are considered there is a range of potential effects, which depend critically on the interspecific scaling relationships of energy gains and energy costs. Since these traits may vary in time, in space, and across species, general predictions from the energetics hypothesis of the direction of selection on body size are therefore not possible, and a wide range of directional effects of latitude on size is therefore predicted (and observed). It is generally the case that, within a species, mass explains less than 50% of the individual variation in metabolic energy expenditure. This low explained variation raises the question of why some individuals sustain high rates of metabolism, when this would be likely to make them more susceptible to failure in achieving an energy balance. In wood mice, Apodemus syluaticus, we have found a correlation between basal metabolic rate (BMR) and the thermogenic capacity (noradrena line-induced metabolic rate). These latter data suggest that animals which might be at a disadvantage in terms of achieving an energy balance might be at an advantage in terms of achieving a heat balance under severe temperature conditions. This indicates a more complex involvement of energetics in the phenomenon of overwinter survivorship than is addressed by models of energy balance alone.
Diet Quality Limits Summer Growth of Field Vole Populations
PLoS ONE, 2014
Marked variation occurs in both seasonal and multiannual population density peaks of northern European small mammal species, including voles. The availability of dietary proteins is a key factor limiting the population growth of herbivore species. The objective of this study is to investigate the degree to which protein availability influences the growth of increasing vole populations. We hypothesise that the summer growth of folivorous vole populations is positively associated with dietary protein availability. A field experiment was conducted over a summer reproductive period in 18 vegetated enclosures. Populations of field voles (Microtus agrestis) were randomised amongst three treatment groups: 1) food supplementation with ad libitum high protein (30% dry weight) pellets, 2) food supplementation with ad libitum low protein (1% dry weight; both supplemented foods had equivalent energy content) pellets, and 3) control (no food supplementation), n = 6 per treatment. Vole density, survival, demographic attributes and condition indicators were monitored with live-trapping and blood sampling. Highest final vole densities were attained in populations that received high protein supplementation and lowest in low protein populations. Control populations displayed intermediate densities.
Winter Food Supply Limits Growth of Northern Vole Populations in the Absence of Predation
Ecology, 2003
Mathematical models have suggested that population cycles of northern voles are generated by a combined effect of delayed and direct density-dependent mechanisms. Predation is considered to be the most likely mechanism affecting vole populations in a delayed density-dependent manner. We conducted a replicated two-factor experiment with the field vole (Microtus agrestis) during 1999-2001 in western Finland, manipulating both predation rate and winter food supply to evaluate whether a shortage of winter food has the potential to limit the growth of vole populations in a direct density-dependent manner. Vole populations in fenced predator exclosures rapidly attained higher densities than in unfenced areas, with the difference persisting until the end of the experiment. In the first winter, food supplementation increased vole population growth in fenced areas, but not in unfenced areas. The growth of vole populations in both supplemented and nonsupplemented fenced areas became limited in a direct density-dependent manner during the first winter. During the second winter, food supplementation prevented the crash of vole populations within fences, whereas again no obvious effect was found in the areas exposed to predation. Furthermore, supplemental winter food increased the overwinter survival of voles in fenced areas in both winters. Our results indicate that Microtus vole populations that have succeeded in escaping regulation by predators are limited in growth by a lack of winter food. This factor is thus a strong candidate for the direct density dependence inherently necessary for the occurrence of population cycles.
2009
Arvicoline rodents (voles and lemmings) inhabit high-latitude environments and undergo pronounced seasonal changes in their physiology and behavior. They are an important prey resource in circumpolar regions, and their population numbers can affect the survival and reproductive fitness o f many predator and secondary prey species. I studied the effects of seasonality and environmental factors on reproduction and energy allocation in the northern red-backed vole (.Myodes rutilus), an arvicoline rodent in Alaska known to have bred in winter. My overall aim was to measure the effects of season and environmental factors on the reproductive axis, body composition, and energy expenditure of this animal. I validated a dual-energy X-ray absorptiometry (DXA) apparatus for use in determining fat and lean tissue, body water, protein, and mineral content in M. rutilus (R2 = 0.65 to 0.98, p < 0.001 for all parameters). Absolute fat, but not percentage fat changed seasonally. Reproductive organ masses reached peak levels in spring (females) and early summer (males), and significant co-variates were photoperiod, temperature, snow cover, body mass, and percent fat (depending on breeding period and gender). I found one instance o f late-summer male non-responsiveness, but no winter breeding. However, 28.2% o f captive, lab-raised male voles were non-responsive to short days {ad lib. food and water at 20°C), which was within the 20-40% frequency range known for lower latitude species. Differences were found at the gonadal level and pituitary level (testosterone and luteinizing hormone (LH) either varied by group and/or were correlated with testis mass), while differences at the hypothalamic level (gonadotropin-releasing hormone immunoreactivity (GnRH-ir) and gonadotropininhibiting hormone (GnlH)-ir cell counts) were inconclusive. Body composition and relative visceral organ mass changed seasonally, and significant covariates were photoperiod (mass, %protein, %mineral), gender (intestines), and temperature (heart). Field metabolic rate did not differ by breeding period, but was significantly correlated with temperature. Bone mineral density (BMD) of voles was highest in early summer and lowest in winter, whereas the BMD o f two hibernating mammals did not change during winter torpor. These findings could help to identify the mechanisms underpinning arvicoline rodent population cycling and to predict physiological and ecological responses of small mammals to different climate change scenarios. invaluable in my education and training. I would especially like to thank Dr. van Tets for funding this research from his grants and for the hours he invested into advising me and revising my manuscripts. Thank you to all of my professors, including Drs. Sasha Kitaysky and Jerry Kudenov. I would like to thank the post docs, graduate and undergraduate students, NIH-NIDDK high school students, and UAA/UAF staff that contributed to the success of this research. Special thanks are due to Fredha Olson, April Brennan, UAF Animal Quarters for the time they invested. I would also like to thank my lab mates and other graduate students that provided laughter and conversation over the years. On a personal note, I would like to thank my wife, Devon, who has supported me, served me, loved me, and endured with me throughout the years of graduate school with unwavering encouragement and limitless grace. Completion of my degrees could not have been possible without your help and patience. I am forever grateful. To my daughter, Moriah, you have been a never-ending source of love and happiness. Thank you for your smiles and hugs that I could count on every day when I returned home. To my parents, James and Janice, and other family members who helped to spur me on to completion, thank you for your encouragement, love, and the opportunities you gave me to succeed. To my church family and friends, thank you for your counsel, prayers, and friendship. You have been precious to me. Finally, to Jesus Christ, my gracious Lord and Savior, you have walked with me every step of the way through this process. I have infinite joy in You. Thank you for loving and dying for this wretched sinner. XV 1 Chapter 1: 'S tevenson K T, van T ets 1G. 2008. D ual-E nergy X-R ay A bsorptiom etry (D X A) can accurately and n o n destructively m easure the body condition o f sm all, free-living rodents. P hysioI B iochem Z ool 81 (3):3 7 1-382.
journal of comparative physiology, 2019
Rodents colonising subterranean environments have developed several morphological, physiological and behaviour traits that promote the success of individuals in such demanding conditions. Resting metabolic rate, thermoregulation capacity and daily energy expenditure were analysed in two semi-fossorial pine-vole species Microtus lusitanicus and Microtus duodecimcostatus inhabiting distinct areas of the Iberian Peninsula. Individuals capture location varied in habitat and soil features, allowing the comparison of energetic parameters with ecological characteristics, that can help explain the use of the subterranean environment and dependence of the burrow system. Results showed that M. duodecimcostatus has lower mass independent resting metabolic rate when compared with M. lusitanicus, which may be a response to environmental features of their habitat, such as dryer soils and lower water availability. Thermal conductance increased with body mass and was dependent on the ambient temperature. No significant differences were observed in the daily energy expenditure, but water economy data demonstrated the influence of the water available in the habitat on the energetics of voles. These species may rely on behavioural adaptations and seasonal use of burrows to cope with thermal challenges of subterranean activity and soil constraints. We found strong evidence that M. lusitanicus is able to use torpor as a response to low ambient temperatures which is a new observation among Arvicolines.