G. J. Kenagy

Size and Function of Mammalian Testes in Relation to Body Size

We have assessed the allometric relationship between mass of testes and body mass using data from 133 mammalian species. The logarithmically transformed data were fitted by a regression ( r 2 = 0.86) that is described by the power function: Y = 0.035X0.72, where Y is mass of both testes in grams and X is body mass in grams. The slopes and intercepts of the allometric relationship for rodents alone (62 species) and primates alone (28 species) do not differ significantly from the relationship for the 133 species all taken together. Smaller mammals must allocate a greater proportion of body mass and of energy expenditure to testicular tissue than larger mammals; according to our allometric equation the testes of a 10 g mammal should comprise 1.8 percent of body mass, whereas testes of a 10,000 kg mammal amount to only 0.04 percent. Among the smallest mammals, the range of relative testes size is great; the testes of some rodents are as large as 8 percent of body mass, whereas others are as small as 0.15 percent. The energy cost for growth, maintenance, and production by mammalian testes is proportional to mass of testes and is, therefore, in most cases negligible. Among mammals in general we found no correlation between size of the testes and their location (abdominal or scrotal) in the body, or between size of testes and body form and mode of locomotion (terrestrial, aquatic, aerial). A functional relationship exists in many mammals between relative size of testes and mating system. Testes are relatively small in single-male breeding systems (monogamy or cases of extreme polygyny in which a single male does all the breeding). Testes are relatively large in multi-male breeding systems (promiscuous or polygynous systems where several different males mate with each female at the same estrus). In these cases, the evolution of large testes can be attributed to high copulatory frequency and sperm production and the competition among sperm of different males for fertilization of the same female. Size of testes has undoubtedly evolved in each species in response to a variety of additional factors beyond the first-order influence of body size. Tests of further hypotheses (for example, degree of seasonality of mating) that may explain the additional variability in size of testes should be performed. This should involve multivariate analyses of large data sets or simpler analyses that use data sets restricted to animals of similar body size, lower-level taxon, mating system, etc.

Annual cycle of energy and time expenditure in a golden-mantled ground squirrel population

SummaryWe have analyzed seasonal shifts of energy and time allocation in a population of golden-mantled ground squirrels (Spermophilus saturatus) by directly measuring total daily energy expenditure (DEE) with an isotopic technique (“doubly labeled water”=dlw), and by estimating components of total DEE through an integration of field behavioral observations with laboratory-measured rates of energy expenditure (oxygen consumption) associated with major behavioral and physiological states. Hibernation laster about 7 1/2 months, and the 4 1/2-month activity season consisted of mating, a 28-d gestation of 3–5 young, 5 1/2 weeks of postnatal growth building to a peak in lactation just before the young emerged above ground, an additional 2–3-week period of maternal care before dispersal, and finally restoration of body mass preceding hibernation. Although the hibernation season comprised nearly two-thirds of the year, it involved only 13–17% of annual energy expenditure, leaving about 85% of energy expenditure for the active season. Ground squirrels were actually present on the surface for only about 11% of the years time, and the foraging time required to obtain the total annual energy supply amounted to only about 2% of the years time. The squirrels fed mainly on herbs in the early season and hypogeous fungi later; both were used extensively during peak lactation when female energy expenditure and demand were maximal. Average daily foraging time increased steadily throughout the season to a maximum of 28% of aboveground time as availability of greens diminished and fungus predominated in the diet; time availability did not limit foraging since the animals sat on average for 65% of the daily surface time of about 7 h. Timing of reproduction is apparently optimized such that peak reproductive energy demands are matched with maximal food availability and moderate thermal conditions that minimize energy demand. Despite the greater body mass of males, the greatest total DEE (measured by dlw) of any squirrels at any time of year was that of females during peak lactation. For production of young and lactation through above-ground emergence of an average litter of 2.7, females required a total energy increase of 24% above annual nonreproductive metabolism. Yearling females all bred and performed similarly to older females, yet some costs were greater because the yearlings began and ended hibernation at smaller mass, compensated by giving birth later, and finally showed a greater absolute increase in body mass over the active season than older females. Annual metabolic energy expenditure of breeding males was about 18% greater than that of females, due to greater male body mass. Yet the annual energy intake requirement for both sexes was essentially identical (about 42MJ) due to the greater reproductive export by females in the form of newborn and milk. During the mating season males showed wide-ranging exploratory behavior and social interactions, including aggression, that involved considerable locomotory energy expenditures. Although we did not directly account for the energetics of these specific reproductive behaviors, they are critical to male reproductive success and on a daily basis they probably involved much greater energy expenditure than sperm production. Some yearling males avoided these costs by foregoing testicular development, yet they allocated four times as much energy to growth as older males, thereby increasing somatic condition for the future.

Seasonal Reproductive Patterns in Four Coexisting Rodent Species from the Cascade Mountains, Washington

We studied annual cycles of three sciurids and one cricetid rodent that coexist in a strongly seasonal environment in the Cascade Mountains of Washington. Spermophilus saturatus (Cascades golden-mantled ground squirrel) hibernated for 6–8 months, whereas Eutamias townsendii (Townsends chipmunk) and E. amoenus (yellow-pine chipmunk) hibernated for only 4–4.5 months. Peromyscus maniculatus (deer mouse) did not hibernate. The three sciurids bred only once a year, with a 1- to 2-week mating period between late March and early May; E. amoenus bred about a month before the other two sciurids. Males emerged from hibernation 1–2 weeks before females, and mating occurred within a week of female emergence. P. maniculatus began breeding in February and continued through October; adult females produced as many as three litters, and the earliest juvenile cohorts reproduced in the year of birth. None of the sciurids became reproductively active until they were yearlings, and some E. townsendii and S. saturatus did not breed until 2 years of age. Average litter size was similar in the four species: S. saturatus , 4.1; E. townsendii , 3.8; E. amoenus , 5.0; and P. maniculatus , 4.6. Because female P. maniculatus bear 2–3 litters per year and juveniles breed in the year of birth, this species has the most flexible timing and greatest annual reproductive potential. The total mass of young produced at the end of gestation and upon emergence from the natal burrow imposes an energetic burden that scales inversely with body mass among the four species. Lipid reserves do not contribute directly to energy requirements of gestation and lactation. Lipid reserves play a major sustaining role during hibernation in S. saturatus (prehibernation body fat >30%), but chipmunks fatten only slightly (body fat < 7%) and rely on food caches during hibernation. P. maniculatus does not fatten substantially. S. saturatus that emerge from hibernation ready to breed contain residual hibernatory fat used for 1–2 weeks as a supplement to ingested food.

Reingestion of feces in rodents and its daily rhythmicity.

SummaryThe ingestion of feces is widespread among rodent species and is an extensively employed component of the repertoire of feeding behaviors in some species. Coprophagy is thus a significant consideration in the nutrition and dietary ecology of many rodents. As certain fecal pellets pass from the anus, they are taken up directly into the mouth, chewed, and swallowed. The nocturnally active herbivorous kangaroo rat Dipodomys microps ingests about 1/4 of the feces it produces daily and the daily pattern of reingestion shows a consistent rhythm. For about 8 h of the daytime, during the non-foraging, resting phase of the day, D. microps reingests all fecal pellets produced; during the remainder of the day it leaves all feces produced. The reingested feces contain more nitrogen and water, and less inorganic ions than the non-reingested feces. The extent of reingestion varies among rodent species in relation to diet, and coprophagy is more important in the more herbivorous species. The granivorous kangaroo rat D. merriami ingests feces rarely. The herbivorous vole Microtus californicus ingests about 1/4 of its feces, as does D. microps. However, in contrast to D. microps, M. californicus shows a series of rhythmic, short-term (one to several hour duration) alternations between reingestion and non-reingestion during the course of the day and night. This pattern correlates with the pattern of foraging in M. californicus, which extends over both night and day.

Energy Costs of Walking and Running Gaits and Their Aerobic Limits in Golden-Mantled Ground Squirrels

We studied locomotion of field-caught golden-mantled ground squirrels (Spermophilus saturatus) on a motorized treadmill that was incorporated into a respirometry system. The animals shifted gaits, from walking to trotting, at about 0.8 m/s and from trotting to galloping at 1.2 m/s; they ran as fast as 3 m/s (10.8 km/h) on our treadmill. Because we were able to determine oxygen consumption instantaneously, we observed rates of energy expenditure that accompany brief bouts of locomotion at speeds higher than those of previous studies. The slope of equations describing oxygen consumption (V̇o2, in ml/g· h) in relation to speed (m/s) differ significantly (P < .02) for walking and running (running = trot and gallop combined): walking (V̇o2 = 2.91 + 3.80 × speed), running (V̇o2 = 5.76 + 1.41 × speed). The animals thereby experience less incremental increase in rate of energy expenditure with increased speed when running than when walking. We conclude that with a maximum aerobic metabolic rate (V̇o2max) of about 10 ml/g · h, which occurs at a speed of 3 m/s, most of the spontaneous running by the ground squirrels observed under natural conditions should occur without the use of anaerobic respiration.

Rates of gut passage and retention of hypogeous fungal spores in two forest dwelling rodents

Alimentary retention of hypogeous fungal spores by small mammals influences the spatial and temporal dynamics of spore dispersal. We investigated, in laboratory experiments, retention of spores of Elaphomyces granulatus by two mycophagous small mammals, the golden-mantled ground squirrel, Spermophilus saturatus , and the deer mouse, Peromyscus maniculatus . The concentration of spores in feces peaked at 20 h and < 12 h after feeding in S. saturatus and P. maniculatus , respectively, but the time for it to fall to half its maximum was similar (approximately 12 h) in both species. Mean retention times of spores were 24 h for S. saturatus and 12 h for P. maniculatus . Alimentary mechanisms that selectively retain small particles such as fungal spores may be common among small mammals, but spores were not retained for longer than the much larger particles of stained alfalfa ( Medicago sativa ) leaf in either S. saturatus or P. maniculatus . Despite the rapid excretion of most spores, the inoculating potential of feces may remain high for many days after cessation of feeding on fungus if large numbers of spores are ingested initially. Fungal spores ingested by S. saturatus immediately before onset of hibernation are excreted slowly, and a significant proportion may remain in the gut throughout hibernation. These could be dispersed in spring when little dispersal might occur otherwise.

Life with fur and without: experimental field energetics and survival of naked meadow voles

Abstract Hair is considered to be a basic mammalian feature that provides protection and insulation, promoting energy conservation and survival. To quantify the functional significance of mammalian pelage, we tested the short-term experimental effects of fur removal in a natural population of the California vole, Microtus californicus, in winter. The daily energy expenditure (DEE) of seven voles was directly measured in the field using stable isotopes, first with the animals in their natural condition and then again after experimental removal of pelage by shaving. The initial mean±SD DEE of 96.0±23.1 kJ/day increased by only about 10%, to 106.3±21.4 kJ/day, following shaving. The voles showed a body mass loss of 5%, about half of which was due to fur removal. Comparing slightly larger samples of all animals whose local survival could be documented, we found 100% survival over the 5 initial days of the experimental manipulation in 16 control animals and nine shaved animals; over the following 3 weeks the survival of shaved mice did not differ significantly from that of controls. We were surprised that the average increase in energy expenditure of voles without fur was so modest, though the range of individual values was great, and likewise we were surprised that shaved voles survived as well as they did. M.californicus survives naturally in winter under conditions of social aggregation that include huddling together of individuals in nests; this situation probably provided our experimentally shaved voles an opportunity to minimize the energetic disadvantages of pelage loss. They may also have employed a variety of compensatory physiological and behavioral responses, including reduction in activity time and food intake, and perhaps a related small decline in body mass. Our limited sample sizes made it difficult to detect subtle differences that may have been biologically significant in the system we studied. Nonetheless, we can reaffirm that fur has an insulative value that promotes energy economy and survival. However, we also conclude that mammalian physiology and behavior are sufficiently complex and flexible that a variety of responses can be deployed to promote survival under unusual circumstances such as those of our experimental test.

Effects of Seed Distribution and Competitors on Seed Harvesting Efficiency in Heteromyid Rodents

SummaryThe foraging strategies of four naturally co-existing heteromyid rodent species were investigated: Dipodomys deserti (≈100 g), D. merriami (≈38 g), Microdipodops pallidus (≈13 g), and Perognathus longimembris (≈7 g). In 208 over-night laboratory foraging trials animals were provided with millet seed distributed in clumped and scattered patterns. Net removal of seeds from the foraging arena and amounts of seeds in cheek pouches and in caches were determined. When alone in an areana none of these species specialized extensively on either clumped or scattered seeds, although each tended to take more clumped than scattered seeds. When placed together with other individuals, animals once again tended to cache more clumped than scattered seeds in all but one paired combination of species: P. longimembris cached more scattered than clumped seeds when opposed by D. deserti. This suggests that the smaller species obtained a less preferred distribution of seeds in the face of competition. The two smaller species showed a great reduction in general foraging success in the presence of either of the two larger species. In general, a species cached less seeds when faced by larger opponent species.

Genetic and phenotypic variation across a hybrid zone between ecologically divergent tree squirrels (Tamiasciurus)

A hybrid zone along an environmental gradient should contain a clinal pattern of genetic and phenotypic variation. This occurs because divergent selection in the two parental habitats is typically strong enough to overcome the homogenizing effects of gene flow across the environmental transition. We studied hybridization between two parapatric tree squirrels (Tamiasciurus spp.) across a forest gradient over which the two species vary in coloration, cranial morphology and body size. We sampled 397 individuals at 29 locations across a 600‐km transect to seek genetic evidence for hybridization; upon confirming hybridization, we examined levels of genetic admixture in relation to maintenance of phenotypic divergence despite potentially homogenizing gene flow. Applying population assignment analyses to microsatellite data, we found that Tamiasciurus douglasii and T. hudsonicus form two distinct genetic clusters but also hybridize, mostly within transitional forest habitat. Overall, based on this nuclear analysis, 48% of the specimens were characterized as T. douglasii, 9% as hybrids and 43% as T. hudsonicus. Hybrids appeared to be reproductively viable, as evidenced by the presence of later‐generation hybrid genotypes. Observed clines in ecologically important phenotypic traits—fur coloration and cranial morphology—were sharper than the cline of putatively neutral mtDNA, which suggests that divergent selection may maintain phenotypic distinctiveness. The relatively recent divergence of these two species (probably late Pleistocene), apparent lack of prezygotic isolating mechanisms and geographic coincidence of cline centres for both genetic and phenotypic variation suggest that environmental factors play a large role in maintaining the distinctiveness of these two species across the hybrid zone.

DIVERSIFICATION AND GENE FLOW IN NASCENT LINEAGES OF ISLAND AND MAINLAND NORTH AMERICAN TREE SQUIRRELS (TAMIASCIURUS)

Pleistocene climate cycles and glaciations had profound impacts on taxon diversification in the Boreal Forest Biome. Using population genetic analyses with multilocus data, we examined diversification, isolation, and hybridization in two sibling species of tree squirrels (Tamiasciurus douglasii and Tamiasciurus hudsonicus) with special attention to the geographically and genetically enigmatic population of T. hudsonicus on Vancouver Island, Canada. The two species differentiated only about 500,000 years ago, in the Late Pleistocene. The island population is phylogenetically nested within T. hudsonicus according to our nuclear analysis but within T. douglasii according to mitochondrial DNA. This conflict is more likely due to historical hybridization than to incomplete lineage sorting, and it appears that bidirectional gene flow occurred between the island population and both species on the mainland. This interpretation of our genetic analyses is consistent with our bioclimatic modeling, which demonstrates that both species were able to occupy this region throughout the Late Pleistocene. The divergence of the island population 40,000 years ago suggests that tree squirrels persisted in a refugium on Vancouver Island at the last glacial maximum, 20,000 years ago. Our observations demonstrate how Pleistocene climate change and habitat shifts have created incipient divergence in the presence of gene flow.