Coupled dynamics of body mass and population growth in response to environmental change.

Environmental change has altered the phenology, morphological traits and population dynamics of many species. However, the links underlying these joint responses remain largely unknown owing to a paucity of long-term data and the lack of an appropriate analytical framework. Here we investigate the link between phenotypic and demographic responses to environmental change using a new methodology and a long-term (1976-2008) data set from a hibernating mammal (the yellow-bellied marmot) inhabiting a dynamic subalpine habitat. We demonstrate how earlier emergence from hibernation and earlier weaning of young has led to a longer growing season and larger body masses before hibernation. The resulting shift in both the phenotype and the relationship between phenotype and fitness components led to a decline in adult mortality, which in turn triggered an abrupt increase in population size in recent years. Direct and trait-mediated effects of environmental change made comparable contributions to the observed marked increase in population growth. Our results help explain how a shift in phenology can cause simultaneous phenotypic and demographic changes, and highlight the need for a theory integrating ecological and evolutionary dynamics in stochastic environments.

Forelimb muscle architecture and myosin isoform composition in the groundhog (Marmota monax).

Scratch-digging mammals are commonly described as having large, powerful forelimb muscles for applying high force to excavate earth, yet studies quantifying the architectural properties of the musculature are largely unavailable. To further test hypotheses about traits that represent specializations for scratch-digging, we quantified muscle architectural properties and myosin expression in the forelimb of the groundhog (Marmota monax), a digger that constructs semi-complex burrows. Architectural properties measured were muscle moment arm, muscle mass (MM), belly length (ML), fascicle length (l(F)), pennation angle and physiological cross-sectional area (PCSA), and these metrics were used to estimate maximum isometric force, joint torque and power. Myosin heavy chain (MHC) isoform composition was determined in selected forelimb muscles by SDS-PAGE and densitometry analysis. Groundhogs have large limb retractors and elbow extensors that are capable of applying moderately high torque at the shoulder and elbow joints, respectively. Most of these muscles (e.g. latissimus dorsi and pectoralis superficialis) have high l(F)/ML ratios, indicating substantial shortening ability and moderate power. The unipennate triceps brachii long head has the largest PCSA and is capable of the highest joint torque at both the shoulder and elbow joints. The carpal and digital flexors show greater pennation and shorter fascicle lengths than the limb retractors and elbow extensors, resulting in higher PCSA/MM ratios and force production capacity. Moreover, the digital flexors have the capacity for both appreciable fascicle shortening and force production, indicating high muscle work potential. Overall, the forelimb musculature of the groundhog is capable of relatively low sustained force and power, and these properties are consistent with the findings of a predominant expression of the MHC-2A isoform. Aside from the apparent modifications to the digital flexors, the collective muscle properties observed are consistent with its behavioral classification as a less-specialized burrower and these may be more representative of traits common to numerous rodents with burrowing habits or mammals with some fossorial ability.

Litter sex composition affects life-history traits in yellow-bellied marmots.

1. The presence of siblings might have long-lasting fitness consequences because they influence the early environment in which an animal develops. Several studies under laboratory conditions have shown long-lasting consequences from the presence of male siblings in utero on morphology and life-history traits. However, in wild animals, such effects of litter sex composition are unexplored. 2. We capitalized on a long-term study of individually marked yellow-bellied marmots (Marmota flaviventris) and documented the effects of weaned litter sex composition and anogenital distance on several life-history and fitness traits. 3. First, we demonstrated that the number of males in a litter influenced anogenital distance. Then, we found that masculinized females, those with larger anogenital distances, were less likely to survive their first hibernation, were more likely to disperse and were less likely to become pregnant and wean young. Males from male-biased litters had lower growth rates, but we failed to detect longer-term consequences. 4. Taken together, our results show profound sex-dependent effects of litter sex composition, probably due to differential prenatal exposure to androgens, in free-living animals. We conclude that masculinization might constitute an alternative mechanism explaining variation in different demographic traits. This finding highlights the importance of studying these maternal effects, and they enhance our concern over the widespread use of endocrine disrupting compounds.

Median liver lobe of woodchuck as a model to study hepatic outflow obstruction: a pilot study.

BACKGROUND: Hepatic vein outflow obstruction represents an important clinical problem in living-liver transplantation. An animal model is required to study the influence of outflow obstruction on the intrahepatic regulation of liver perfusion and the subsequent effects on liver injury and recovery during liver regeneration. The size of woodchucks enables the use of standard clinical imaging procedures. AIM: This study aims at describing hepatic vascular and territorial anatomy of the woodchuck liver based on a virtual three-dimensional (3D) visualization of the hepatic vascular tree. METHODS: Woodchucks (n=6) were subjected to an all-in-one computed tomography (CT) after contrasting the vascular and the biliary tree. CT-images were used for 3D-reconstruction of hepatic and portal veins and calculation of the corresponding portal and hepatic vein territories and their respective volume using hepavision (MeVisLab). A virtual resection was performed following the Cantlie-line and territories at risk were calculated. RESULTS: The median lobe of the woodchuck liver has a similar vascular supply and drainage as the human liver with two portal (right and left median portal vein) and three hepatic veins (left, middle and right median hepatic vein). The corresponding portal and hepatic vein subterritories are of a similar relative size compared with the human liver. Virtual splitting of the median lobe of the woodchuck liver revealed areas at risk of focal outflow obstruction, as observed clinically. CONCLUSION: The median liver lobe of the woodchuck represents, to a small extent, the hepatic vascular anatomy of the human liver and is therefore a suitable potential model to correlate repeated imaging of impaired liver perfusion with histomorphological findings of liver damage and regeneration.

Phylogenetic and environmental components of morphological variation: skull, mandible, and molar shape in marmots (Marmota, Rodentia).

The phenotype is a product of its phylogenetic history and its recent adaptation to local environments, but the relative importance of the two factors is controversial. We assessed the effects of diet, habitat, elevation, temperature, precipitation, body size, and mtDNA genetic divergence on shape variation in skulls, mandibles, and molars, structures that differ in their genetic and functional control. We asked whether these structures have adapted to environment to the same extent and whether they retain the same amount of phylogenetic signal. We studied these traits in intra- and interspecific populations of Eurasian marmots whose last common ancestor lived 2-5 million years ago. Path Analysis revealed that body size explained 10% of variation in skulls, 7% in mandibles, and 15% in molars. Local vegetation explained 7% of variation in skulls, 11% in mandibles, and 12% in molars. Dietary category explained 25% of variation in skulls, 11% in mandibles, and 9% in molars. Cyt b mtDNA divergence (phylogeny) explained 15% of variation in skulls, 7% in mandibles, and 5% in molars. Despite the percentages of phylogenetic variance, maximum-likelihood trees based on molar and skull shape recovered most phylogenetic groupings correctly, but mandible shape did not. The good performance of molars and skulls was probably due to different factors. Skulls are genetically and functionally more complicated than teeth, and they had more mathematically independent components of variation (5-6-in skulls compared to 3-in molars). The high proportion of diet-related variance was not enough to mask the phylogenetic signal. Molars had fewer independent components, but they also have less ecophenotypic variation and evolve more slowly, giving each component a proportionally stronger phylogenetic signal. Molars require larger samples for each operational taxonomic unit than the other structures because the proportion of within-taxon to between-taxon variation was higher. Good phylogenetic signal in quantitative skeletal morphology is likely to be found only when the taxa have a common ancestry no older than hundreds of thousands or millions of years (1% to 10% mtDNA divergence)--under these conditions skulls and molars provide stronger signal than mandibles.

Seasonal ultrastructural variations in pinealocytes of the woodchuck, Marmota monax.

The ultrastructure of the pinealocyte in the woodchuck, Marmota monax, was studied during the four seasons of the year. Fall cells have a fairly uniform cytoplasmic density, organelles consistent with synthetic and/or secretory activity and rather extensive pericapillary and intercellular spaces. Many winter pinealocytes are nearly devoid of ribosomes and granular endoplasmic reticulum but contain lipid droplets associated with mitochondria. Pericapillary and intercellular spaces are minimal. Spring glands have the greatest variation in cytoplasmic density with intercellular and pericapillary spaces similar to that seen in fall glands. Cells containing electron dense cytoplasm have Golgi zone associated, secretory granules, free ribosomes, short sections of granular endoplasmic reticulum and dense bodies. Cells with a more electron lucent cytoplasm are similar to the most frequently observed summer pinealocytes which have numerous Golgi zones but few associated secretory granules. Microtubules are prominent in the cytoplasm of these cells, the plasma membranes are smooth and intercellular and pericapillary spaces are minimal. A yearly rhythm or cyclic activity of the pinealocyte is suggested.

Incisal biting in the mountain beaver (Aplodontia rufa) and woodchuck (Marmota monax).

Analysis of synchronously recorded cine-radiographs and electromyograms in two rodents (Aplodontia rufa and Marmota monax) demonstrates that jaw movements and muscle activities during incisal functions are distinctly different from those found during mastication. Movements during incisal biting are primarily along the midline, accompanied by symmetrical activity of the jaw adductor muscles. Most biting cycles do not end in contact between upper and lower incisors. When contact does occur, the lower incisors are dragged along the lingual surfaces of the upper incisors. Cropping, or tip-to-tip occlusion of upper and lower incisors, was not observed. Sharpening of the lower incisors, a behavior which may be unique to the Rodentia, was recorded in both A. rufa and M. monax. During sharpening, the lingual surface of the lower incisor is dragged across the tip of the upper incisor producing a lingual wear facet. Like incisal biting, sharpening movements are primarily confined to the midline, although there may be lateral movements in some sharpening cycles. Sharpening cycles are among the most rapid cyclic movements recorded in mammals, as the mean frequencies of sharpening are 11 cycles/s in A. rufa and 8 cycles/s in M. monax.

The parathyroid gland of the woodchuck (Marmota monax): a study of seasonal variations in the chief cells.

The ultrastructure of the parathyroid chief cell in the woodchuck, Marmota monax, was studied during the four seasons of the year. Spring chief cells have stacks of granular endoplasmic reticulum, prominent multiple Golgi zones and many clumped mitochondria. Summer cells resemble those seen in the spring but the mitochondria are associated with stacks of granular endoplasmic reticulum. Multiple areas of stacked granular endoplasmic reticulum characterize the fall chief cells. Their Golgi zones are large and are associated with many dense core secretory granules. Lipoid vacuoles are frequently noted. Winter chief cells have secretory granules and phagolysosomes (dense bodies). Some of these cells contain stacked arrays of granular endoplasmic reticulum associated with mitochondria, others have only short segments. The above morphological findings are discussed in relation to those in other hibernators, the parafollicular (C) cell, and to the cyclic seasonal activities of the woodchuck.

Intracytoplasmic neuronal inclusions in woodchuck brain stem.

Homogenous eosinophilic intracytoplasmic inclusion bodies were found within the large reticular neurons of the brain stems of 57 captive woodchucks (Marmota monax). Light microscopy was consistent with a proteinaceous nature, while electron microscopy suggested a non-viral origin. The woodchucks with inclusions were older than the general population that was studied. It is hypothesized that the neuronal inclusions in the brain stem are indicative of nonspecific ageing changes.

The bronchial tree, lobular division and blood vessels of the woodchuck (Marmota monax) lung.

The right lung of the woodchuck (Marmota monax) consists of the upper, middle, lower and accessory lobes, which are separated by interlobular fissures. The left lung consists of the middle and lower lobes, which are united to form a single lobe. In one of the two specimens examined, the left lung had a small upper lobe bronchiole. The right pulmonary artery runs along the ventrolateral side of the right bronchus crossing the ventral side of the right upper lobe bronchiole, then crosses the dorsal side of the right middle lobe bronchiole, and thereafter runs between the dorsal and lateral bronchiole systems, along the dorsolateral side of the right bronchus. During its course, the right pulmonary artery gives off branches which run along each bronchiole, mainly on the dorsal or lateral side. The left pulmonary artery runs across the dorsal side of the left middle lobe bronchiole and is distributed to the left middle and lower lobes in a manner similar to the right pulmonary artery in the right middle and lower lobes. The pulmonary veins run mainly along the medial or ventral side of the bronchioles, and between them.

Maternal effects on anogenital distance in a wild marmot population.

In mammals, prenatal exposure to sex steroid hormones may have profound effects on later behavior and fitness and have been reported under both laboratory and field conditions. Anogenital distance is a non-invasive measure of prenatal exposure to sex steroid hormones. While we know that intra-uterine position and litter sex ratio influence anogenital distance, there are other, heretofore unstudied, factors that could influence anogenital distance, including maternal effects. We capitalized on a long-term study of wild yellow-bellied marmots (Marmota flaviventris) to study the importance of maternal effects on explaining variation in anogenital distance and found significant effects. The strength of these effects varied annually. Taken together, our data highlights the strong variability due to environmental effects, and illustrates the importance of additive genetic and maternal genetic effects on neonatal anogenital distance. We suspect that, as others apply recently popularised quantitative genetic techniques to study free-living populations, such effects will be identified in other systems.

Yellow-bellied marmots: insights from an emergent view of sociality.

Ecological factors explain variation in sociality both within and between species of marmots-large alpine ground squirrels. Fifty years of study, by me and my colleagues, of the yellow-bellied marmots (Marmota flaviventris) at the Rocky Mountain Biological Laboratory, near Crested Butte, CO, USA, has created opportunities to see how sociality changes with population and group size. Over the past decades, we have witnessed a natural experiment whereby the population tripled in size. If we view sociality as an emergent process, then demography acts as a constraint on interactions between individuals, and the threefold increase in population size should have consequences for group structure. We have used social network statistics to study the causes and consequences of social interactions by capitalizing on this demographic variation. Such an emergent view is ideally studied in an integrative Tinbergian way that focuses on both mechanism and function. We have determined that some social attributes are heritable, that social cohesion is established through age and kin structure, that well-embedded females (but not males) are less likely to disperse, and that there are fitness consequences of social attributes. Together, this integrative relationship-centred view expands on the traditional ecological model of sociality and offers a framework that can be applied to other systems.

Yellow-bellied marmots (Marmota flaviventris) preserve bone strength and microstructure during hibernation.

Reduced skeletal loading typically results in decreased bone strength and increased fracture risk for humans and many other animals. Previous studies have shown bears are able to prevent bone loss during the disuse that occurs during hibernation. Studies with smaller hibernators, which arouse intermittently during hibernation, show that they may lose bone at the microstructural level. These small hibernators, like bats and squirrels, do not utilize intracortical remodeling. However, slightly larger mammals like marmots do. In this study we examined the effects of hibernation on bone structural, mineral, and mechanical properties in yellow-bellied marmots (Marmota flaviventris). This was done by comparing cortical bone properties in femurs and trabecular bone properties in tibias from marmots killed before hibernation (fall) and after hibernation (spring). Age data were not available for this study; however, based on femur length the post-hibernation marmots were larger than the pre-hibernation marmots. Thus, cross-sectional properties were normalized by allometric functions of bone length for comparisons between pre- and post-hibernation. Cortical thickness and normalized cortical area were higher in post-hibernation samples; no other normalized cross-sectional properties were different. No cortical bone microstructural loss was evident in osteocyte lacunar measurements, intracortical porosity, or intracortical remodeling cavity density. Osteocyte lacunar area, porosity, and density were surprisingly lower in post-hibernation samples. Trabecular bone volume fraction was not different between pre- and post-hibernation. Measures of both trabecular and cortical bone mineral content were higher in post-hibernation samples. Three-point bending failure load, failure energy, elastic energy, ultimate stress, and yield stress were all higher in post-hibernation samples. These results support the idea that, like bears, marmots are able to prevent disuse osteoporosis during hibernation, thus preventing increased fracture risk and promoting survival of the extreme environmental conditions that occur in hibernation.

Evolutionary acceleration in the most endangered mammal of Canada: speciation and divergence in the Vancouver Island marmot (Rodentia, Sciuridae).

The Vancouver Island marmot is the most endangered mammal of Canada. Factors which have brought this population to the verge of extinction have not yet been fully elucidated, but the effects of deforestation and habitat fragmentation on survival rates, as well as those of variation in rainfall, temperature, snowpack depth and snowmelt strongly suggest that marmots on the island are struggling to keep pace with environmental changes. Genetic analyses, however, seem to indicate that the Vancouver Island marmot may merely represent a melanistic population of its parental species on the mainland. Were it not for its black pelage colour, it is unlikely that it would have attracted much attention as a conservation priority. Our study uses three-dimensional coordinates of cranial landmarks to further assess phenotypic differentiation of the Vancouver Island marmot. A pattern of strong interspecific divergence and low intraspecific variation was found which is consistent with aspects of drift-driven models of speciation. However, the magnitude of shape differences relative to the putatively neutral substitutions in synonymous sites of cytochrome b is too large for being compatible with a simple neutral model. A combination of bottlenecks and selective pressures due to natural and human-induced changes in the environment may offer a parsimonious explanation for the large phenotypic differentiation observed in the species. Our study exemplifies the usefulness of a multidisciplinary approach to the study of biological diversity for a better understanding of evolutionary models and to discover aspects of diversity that may be undetected by using only a few genetic markers to characterize population divergence and uniqueness.

Seasonal changes in the ultrastructure of the thyrotroph in the wookchuck (Marmota monax) adenohypophysis.

Throtrophs of the woodchuck anterior pituitary are described through the four seasons of the year. Evidence of an increase in number and activity in the spring is presented. Activity of the thyrotroph is seen to continue through the summer and decline in the autumn to quiescence during the hibernatory period of winter. The significance of these findings is discussed in relation to thyoid follicular cell morphology, serum T3 and T4 levels and the physiological activities of the animal. High levels of thyroid hormones in the serum may be consistent with the appearance of great activity seen in the thyrotroph and follicular cell when taken in context with breeding season, ambient temperature and lack of food.

The thyroid gland of the woodchuck, Marmota monax: a morphological study of seasonal variations in the follicular cells.

The morphology of the thyroid gland of the woodchuck, Marmota monax, was studied during the four seasons of the year. In the spring the thyroid is extremely heterogenous in appearance. Some follicular cells appear quite active. They contain a well defined Golgi apparatus, abundant large colloid droplets and pseudopodia but few, if any, apical vesicles. Other less active cells have poorly defined rough surfaced endoplasmic reticulum and lack a well developed Golgi apparatus. They do not contain apical vesicles or colloid droplets. Summer thyroids have uniformly small follicles which are lined by high cuboidal cells containing numerous mitochondria, apical vesicles, abundant rough surfaced endoplasmic reticulum, and lipid droplets but few colloid droplets. There is extensive lateral and basal infolding of the cytoplasmic membranes in these cells. In the fall and winter the follicles are larger than in the summer and contain more colloid. Numerous heterogeneous dense bodies appear in the cytoplasm of the follicular cells in the fall and increase in number in the winter when there is an obvious sparsity of such glycoprotein synthetic organelles as Golgi apparatus and rough surfaced endoplasmic reticulum. These morphologic changes are compared with previous studies of thyroid structure and function in other animals and are correlated with the seasonal physiologic activities of the woodchuck.