Hibernating patterns of free-ranging Columbian ground squirrels

Summary The patterns of torpor and euthermy during hibernation was documented for 28 free-ranging Columbian ground squirrels (Spermophilus columbianus) fitted with temperature-sensitive radio transmitter collars. Adult males began hibernation earlier, were euthermic for a greater proportion of the hibernating season and emerged earlier than other age and sex classes. The patterns of hibernation of adult females did not differ significantly from those of juveniles. Emergence from the hibernaculum was preceded by a long (3–12 d) euthermic interval in adult males but not in adult females or juveniles. Changes in soil temperature did not appear to initiate emergence. The greater time spent euthermic by adult males is interpreted as a significantly greater energy cost of hibernation for adult males than for other age and sex classes. The benefits offsetting these costs may be increased reproductive potential in spring and avoidance of predation in late summer.     

High gene flow between populations of Macrotermes michaelseni (Isoptera, Termitidae)

Termite alates are thought to be poor active flyers, and this should lead to considerable genetic differentiation on small spatial scales. However, using four microsatellite loci for the termite Macrotermes michaelseni we found low values of genetic differentiation (F_ST) across a spatial scale of even more than 50 km. Genetic differentiation between populations increased with spatial distance up to 50 km. Furthermore, up to this distance, the scatter around the linear regression of genetic differentiation versus spatial distance increased with spatial distance. This suggests that across such spatial distances gene flow and genetic drift are of about equal importance, and near equilibrium. Using a regional F_ST as well as the distance between populations with non-significant F_ST-values (up to 25 km), gene flow is sufficiently high so that populations may be regarded as panmictic on spatial scales of 25 to 50 km. The apparent contradiction between dispersal distances observed in the field and estimates of gene flow from genetic markers may be due to the masses of swarming alates. Assuming a leptokurtic distribution of dispersal distances, atleast some alates are expected to travel considerable distances, most likely by passive drift. Received 25 January 2005; revised 11 April 2005; accepted 26 April 2005.     

Regulation of population size: evidence from Columbian ground squirrels

The hypothesis that food resources regulate population size was tested in Columbian ground squirrels, Spermophilus columbianus, from 1981 to 1986 in southwestern Alberta, Canada. Two replicate populations received supplemental food resources from 1981 to 1983, and were subsequently monitored until 1986. Two reference (unmanipulated) populations were monitored throughout the 6 years. During the experiment, dramatic increases in population size of about 500% occurred. After supplementation, spring populations declined by about 20% per year, under conditions that produced stressful shortages of food (as evidenced by significant decreases in body mass of ground squirrels). The demographic process that contributed most to increasing and decreasing experimental populations was production of yearlings, through changes in reproductive success and survival of young. Changes in migration contributed secondarily to changes in population size, and changes in adult survival were least important. While similarities of demographic processes were evident between replicates during population increases, a dramatic decrease in survival of young contributed to population decline at one replicate, and normal levels of reproduction and survival were sufficient to produce a decline in the other replicate. Demographic mechanisms may vary, but population regulation of mammalian populations appears strongly dependent on food resources.     

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

Summary We 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 year's time, and the foraging time required to obtain the total annual energy supply amounted to only about 2% of the year's 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.     

Heterogeneous selection in subdivided populations

The dynamics of allele frequencies changing under migration and heterogeneous selection in a subdivided population are investigated. Using perturbation techniques, a stationary state is obtained when migration and selection are both small. Heterogeneous selection leads to a positive correlation between values of F-statistics and heterozygosities when these are compared among sets of subdivided populations. This contrasts with a negative value of the correlation obtained under Wright's classical model of homogeneous selection, and with the absence of correlation in the completely neutral situation.Research supported in part by NIH grants GM 28016 and GM 10452 and a grant from the John D. and Catherine T. MacArthur Foundation     

Parasites promote host gene flow in a metapopulation

Local adaptation is a powerful mechanism to maintain genetic diversity in subdivided populations. It counteracts the homogenizing effect of gene flow because immigrants have an inferior fitness in the new habitat. This picture may be reversed in host populations where parasites influence the success of immigrating hosts. Here we report two experiments testing whether parasite abundance and genetic background influences the success of host migration among pools in a Daphnia magna metapopulation. In 22 natural populations of D. magna, immigrant hosts were found to be on average more successful when the resident populations experienced high prevalences of a local microsporidian parasite. We then determined whether this success is due to parasitism per se, or the genetic background of the parasites. In a common garden competition experiment, we found that parasites reduced the fitness of their local hosts relatively more than the fitness of allopatric host genotypes. Our experiments are consistent with theoretical predictions based on coevolutionary host-parasite models in metapopulations. A direct consequence of the observed mechanism is an elevated effective migration rate for the host in the metapopulation.     

Sciurid phylogeny and the paraphyly of Holarctic ground squirrels (Spermophilus)

The squirrel family, Sciuridae, is one of the largest and most widely dispersed families of mammals. In spite of the wide distribution and conspicuousness of this group, phylogenetic relationships remain poorly understood. We used DNA sequence data from the mitochondrial cytochrome b gene of 114 species in 21 genera to infer phylogenetic relationships among sciurids based on maximum parsimony and Bayesian phylogenetic methods. Although we evaluated more complex alternative models of nucleotide substitution to reconstruct Bayesian phylogenies, none provided a better fit to the data than the GTR+G+I model. We used the reconstructed phylogenies to evaluate the current taxonomy of the Sciuridae. At essentially all levels of relationships, we found the phylogeny of squirrels to be in substantial conflict with the current taxonomy. At the highest level, the flying squirrels do not represent a basal divergence, and the current division of Sciuridae into two subfamilies is therefore not phylogenetically informative. At the tribal level, the Neotropical pygmy squirrel, Sciurillus, represents a basal divergence and is not closely related to the other members of the tribe Sciurini. At the genus level, the sciurine genus Sciurus is paraphyletic with respect to the dwarf squirrels (Microsciurus), and the Holarctic ground squirrels (Spermophilus) are paraphyletic with respect to antelope squirrels (Ammospermophilus), prairie dogs (Cynomys), and marmots (Marmota). Finally, several species of chipmunks and Holarctic ground squirrels do not appear monophyletic, indicating a need for reevaluation of alpha taxonomy.     

Energetics of arousal episodes in hibernating arctic ground squirrels

Arctic ground squirrels overwintering in northern Alaska experience average soil temperature of −10°C. To examine energetic costs of arousing from hibernation under arctic compared to temperate conditions, captive ground squirrels were maintained in ambient temperatures (T _a) of 2, −5 and −12°C. Rates of oxygen consumption and carbon dioxide production were used to estimate metabolic rate and fuel use during the three phases of arousal episodes: rewarming, euthermia, and recooling. Respiratory quotient comparisons suggest exclusive use of lipid during rewarming and mixed fuel use during euthermia. Animals rewarming from torpor at T _a −12°C took longer, consumed more oxygen, and attained higher peak rates of oxygen consumption when compared to 2°C. T _a had no significant effect on cost or duration of the euthermic phase. Animals recooled faster at −12°C than at 2°C, but total oxygen consumption was not different. T _a had no significant effect on the total cost of arousal episodes when all three phases are included. Arousal episodes account for 86% of estimated costs of a complete hibernation cycle including torpor when at 2°C and only 23% at −12°C. Thus, due to the higher costs of steady-state metabolism during torpor, proportional metabolic costs of arousal episodes at T _a characteristic of the Arctic are diminished compared to relative costs of arousals in more temperate conditions.     

Changes in landscape structure decrease mortality during migration

I examined the dispersal of the red milkweed beetle, Tetraopes tetraophthalmus, among patches of its host plant, common milkweed, Asclepias syriaca. Over a 5-year period, the number of patches in a landscape and their mean size increased, while the distance between patches decreased. Over the same period the proportion of beetles dispersing between patches increased from 0.48 to 0.62. Estimates from the virtual migration model showed that mean migration distance decreased from 158 to 72 m for male beetles and from 129 to 72 m for female beetles. Estimated mortality per migration event decreased as the landscape changed, but was low in all years. The estimated mean migration mortality per patch decreased from 1.45 × 10⁻² to 3.70 × 10⁻⁷ for male beetles. Female migration mortality decreased from 5.48 × 10⁻³ to 3.88 × 10⁻⁶. Increasing the size and number of patches and decreasing interpatch distance decreases migration mortality and may play an important role in the conservation of species, particularly where mortality during dispersal is high.     

Impact of habitat fragmentation on genetic population structure of roach, Rutilus rutilus, in a riparian ecosystem

During the last 200 years, the riparianecosystem along major rivers has been reducedto a few scattered remnants. Important elementsof the riparian ecosystem are water bodieswhich were originally connected to the mainriver channel by annual floodings. Due to riverregulations many of these remnants are nowvirtually isolated. In an allozyme analysisusing roach, Rutilus rutilus, as a studyspecies we demonstrate that the geneticdiversity (number of alleles per locus,expected heterozygosity) of populations livingwithin floodplain water bodies is not severelyimpoverished compared to the genetic diversitywithin the main river channel. However, wefound slight differences in the allelefrequencies of flood plain water bodies and themain river channel. Nevertheless, fishpopulations in floodplain water bodies mayserve as reservoirs of autochthonous geneticmaterial for restoration of fish populations inthe main river channel after populationextinction due to catastrophic accidents (e.g.industrial pollution).     

Cytosolic phospholipase A2 regulation in the hibernating thirteen-lined ground squirrel

Cytosolic calcium-dependent phospholipase A₂ (cPLA₂) has multiple roles including production of arachidonic acid (a key player in cellular signaling pathways) and membrane remodeling. Additionally, since catabolism of arachidonic acid generates free radicals, the enzyme is also implicated in ischemic injury to mammalian organs. Regulation of cPLA₂ could be important in the suppression and prioritization of cellular pathways in animals that undergo reversible transitions into hypometabolic states. The present study examines the responses and regulation of cPLA₂ in skeletal muscle and liver of hibernating thirteen-lined ground squirrels, Spermophilus tridecemlineatus. cPLA₂ activity decreased significantly by 43% in liver during hibernation, compared with euthermic controls, and K_m values for arachidonoyl thio-PC substrate fell in both organs during hibernation to 61% in liver and 28% in muscle of the corresponding euthermic value. To determine whether these responses were due to a change in the phosphorylation state of the enzyme, Western blotting was employed using antibodies recognizing phospho-Ser⁵⁰⁵ on α-cPLA₂. The amount of phosphorylated α-cPLA₂ in hibernator liver was just 38% of the value in euthermic liver. Furthermore, incubation of liver extracts under conditions that enhanced protein phosphatase action caused a greater reduction in the detectable amount of phospho-Ser⁵⁰⁵ enzyme content in euthermic, versus hibernator, extracts. The data are consistent with a suppression of cPLA₂ function during torpor via enzyme dephosphorylation, an action that may contribute to the well-developed ischemia tolerance and lack of oxidative damage found in hibernating species over cycles of torpor and arousal.     

The hypothalamo-hypophysial system in the ground squirrel,Citellus erythrogenys Brandt

Summary Monthly observations of the Gomori-positive hypothalamo-hypophysial neurosecretory system (HHNS) of the ground squirrel, Citellus erythrogenys Brandt, were carried out light microscopically using several quantitative methods. From the beginning of hibernation, formation of neurosecretory material (NSM) in the neurosecretory cells (NSC) progressively decreases and release of neurohormones from the HHNS is almost fully inhibited. A maximal accumulation of NSM in the perikarya of the NSC and in the posterior pituitary (PP) is found in December. By this time the volume of the cell nuclei and nucleoli is at a minimum. Signs of activation of the HHNS appear and become more conspicuous as the time of arousal from torpor approaches. The amount of NSM in the NSC and the PP decreases simultaneously with the increase in volume of the NSC. Hyperemia and activation of glial elements is visible throughout the HHNS. The morphological signs of activation reach their peak in March. After reproduction is completed (April to beginning of May), the NSC and the PP are almost devoid of NSM. Beginning with June and during the summer and autumn months a progressive accumulation of NSM in the NSC and the PP parallels gradual diminution in the volume of the NSC structures and the glial cells. Mechanisms and effector pathways by which the HHNS influences seasonal adaptation of the organism and reproduction are discussed.     

Mechanisms of glycolytic control during hibernation in the ground squirrel Spermophilus lateralis

Summary The mechanisms of glycolytic rate control during hibernation in the ground squirrel Spermophilus lateralis were investigated in four tissues: heart, liver, kidney, and leg muscle. Overall glycogen phosphorylase activity decreased significantly in liver and kidney to give 50% or 75% of the activity found in the corresponding euthermic organs, respectively. The concentration of fructose-2,6-bisphosphate (F-2,6-P₂) decreased significantly in heart and leg muscle during hibernation to 50% and 80% of euthermic tissue concentrations, respectively, but remained constant in liver and kidney. The overall activity of pyruvate dehydrogenase (PDH) in heart and kidney from hibernators was only 4% of the corresponding euthermic values. Measurements of phosphofructokinase (PFK) and pyruvate kinase (PK) kinetic parameters in euthermic and hibernating animals showed that heart and skeletal muscle had typical rabbit skeletal M-type PFK and M₁-type PK. Liver and kidney PFK were similar to the L-type enzyme from rabbit liver, whereas liver and kidney PK were similar to the M₂ isozyme found primarily in rabbit kidney. The kinetic parameters of PFK and PK from euthermic vs hibernating animals were not statistically different. These data indicate that tissue-specific phosphorylation of glycogen phosphorylase and PDH, as well as changes in the concentration of F-2,6-P₂ may be part of a general mechanism to coordinate glycolytic rate reduction in hibernating S. lateralis.Abbreviations ADP adenosine diphosphate - AMP adenosine monophosphate - ATP adenonine triphoshate - EDTA ethylenediaminetetra-acetic acid - EGTA ethylene glycol tetra-acetic acid - F-6-P fructose 6-phosphate - F-1,6-P₂ fructose 1,6-bisphosphate - F-2,6-P₂ fructose-2,6-bisphosphate - K _a activation coefficient - I₅₀ concentration of inhibitor which reduces control activity by 50% - PDH pyruvate dehydrogenase - PEP phosphoenolpyruvate - PFK 6-phosphofructo-1-kinase - PK pyruvate kinase     

A comparative study of embryonic gene expression inDrosophila andEphestia

Summary The ontogeny of allozyme patterns has been studied in embryos ofDrosophilamelanogaster, which are doubly heterozygous for alleles specifying the slow and fast forms of alcohol dehydrogenase (ADH) and -glycerophosphate dehydrogenase (GPDH). The ontogeny of esterase-2 was studied in embryos and young larvae of the flour mothEphestia kühniella, which are heterozygous for two of the three existing esterase-2 alleles. In freshly laidDrosophila eggs only the maternal enzyme forms are present and during the first 15 hours of development the staining of these forms becomes progressively fainter. After 16 and 17 h, the paternal and hybrid bands of ADH and GPDH respectively become obvious. Before hatching, the intensity distribution in the three-banded pattern of reciprocal hybrids is asymmetric in favour of the persisting maternal enzyme form. InEphestia embryos, however, there is no persistence of the maternal esterases. In all reciprocal heterozygotes a three-banded pattern suddenly appears 96 h after egg deposition, indicating synchronous activation of both parental alleles. The relative intensity distribution in the hybrid patterns approaches that of the mature larvae stepwise and in an allele-specific manner. This result and the fact that the various heterozygous types exhibit unequal total activities suggest that the Esterase-2 alleles have different activities, which are fixed late in embryogenesis.     

Multigenic and morphometric differentiation of ground squirrels (Spermophilus, Scuiridae, Rodentia) in Turkey, with a description of a new species

This study reports on the molecular phylogenetics of ground squirrels, genus Spermophilus, in Turkey using cytochrome b (1140bp), part of the D-loop and flanking tRNAs (572bp), X chromosome (867-1051bp) and Y chromosome (983-989bp) DNA sequences. Individuals also were characterized by karyotype and with geometric morphometric analyses of mandibles and skulls. Two hundred fourteen individuals from 91 localities were studied. All the data support the recognition of a new species in SW Anatolia: the Taurus ground squirrel Spermophilus taurensis sp. nov. The new species has a small distribution in the Taurus Mountains in an area that is a hotspot for biodiversity. Molecular clock analysis suggests that the new species diverged from the European ground squirrel, Spermophilus citellus, about 2.5 million years ago and that the ancestor of these two species diverged from the widespread Anatolian ground squirrel, Spermophilus xanthoprymnus, about 5 million years ago. Morphometric differentiation in skull and mandible shape among the three species is incomplete, but statistically significant. S. xanthoprymnus is subdivided into five cytochrome b phylogroups and we use these data to infer the location of glacial refugia where the species lived during the last glacial maximum. This study illustrates the potential of combined molecular and morphometric studies to uncover new Anatolian species and to reconstruct their phylogeographic history. The new species is important for squirrel taxonomy and for understanding Eurasian mammal evolution.     

Daily rhythmicity and hibernation in the Anatolian ground squirrel under natural and laboratory conditions

We studied daily rhythmicity of body temperature (T _b) before and during hibernation in Anatolian ground squirrels (Spermophilus xanthoprymnus) under natural and laboratory conditions using surgically implanted temperature loggers. Under both conditions, robust daily T _b rhythmicity with parameters comparable to those of other ground squirrel species was observed before but not during hibernation. Euthermic animals had robust daily T _b rhythms with a mean of 37.0°C and a range of excursion of approximately 4°C. No T _b rhythm was detected during torpor bouts, either because T _b rhythmicity was absent or because the daily range of excursion was smaller than 0.2°C. The general patterns of hibernation that we observed in Anatolian ground squirrels were similar to those previously observed by other investigators in other species of ground squirrels.     

Developmental and geographic variation in stress hormones in wild Belding's ground squirrels (Spermophilus beldingi)

Extensive research has been conducted on the role of glucocorticoids in regulating growth, mobilizing energy, responding to stressors and modulating learning and memory. However, little is known about the production of corticoids during early development in free-living animals, particularly during sensitive periods of acquisition of important behaviors. In a four-year study of Belding's ground squirrels, Spermophilus beldingi, a non-invasive assay of glucocorticoids was used to quantify age and population differences among juveniles from three California locations. Fecal-cortisol metabolites are elevated during a short period when juveniles first emerge aboveground from their natal burrows at about 4 weeks of age. This period of cortisol elevation coincides with when young are learning survival behaviors such as anti-predator responses and foraging strategies. Population differences in juvenile cortisol levels, which may reflect local variation in habitat quality and predator environments, were not evident until 2 weeks after emergence. Elevated cortisol at the age of emergence was also observed in juveniles born and reared in captivity without exposure to typical stressors that occur around the age of emergence. These results indicate that corticoids are regulated during early development, and the possible functions of age-related corticoid levels are discussed, including mobilization of glucose for natal emergence and later facilitation of growth and energy storage during the short summer before hibernation. In some species, elevated corticoids can also facilitate learning and memory, and current work is exploring whether the higher cortisol observed in all three S. beldingi populations just after emergence function to promote rapid acquisition of survival behaviors.     

Host races and sympatric speciation in small ermine moths, Yponomeutidae

The amount of genetic differentiation at various levels of evolutionary divergence (conspecific populations, sibling species and non-sibling species) in Yponomeuta was determined. Genetic distances between siblings or non-siblings were found to cover a wide range. It is concluded that such estimates do not give much information on the speciation process itself. Inbreeding coefficients were calculated for populations of Y. padellus from a total of six host plants. The grand mean F _ST value is 0.030±0.012. F _ST values for populations sampled from Crataegus, the common food plant of Y. padellus, are 2–3.5 times smaller than those for populations from the other food plants taken together. Host race formation, as measured by significant differences in allozyme frequencies between sympatric populations on two or more food plants, was investigated in four areas. Host race formation seems to occur in Y. padellus and sympatric speciation is a likely event.

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Résumé Le degré de différenciation génétique en allozymes à des niveaux divers de divergence évolutive (populations conspécifiques, sibling species et non-sibling species) d'Yponomeuta a été déterminé. Les distances génétiques entre des sibling species ou des non-sibling species sont très larges. Il en est conclu que de telles estimations ne fournissent pas beaucoup d'informations sur le phénomène de spéciation même. Des coéfficients de reproduction consanguine (F _ST) ont été calculés pour des populations d'Y. padellus provenant de six plantes-hôtes. La valeur moyenne F _STest .030±.012. Les valuers de F _ST des populations recueillies sur Crataegus, (plante-hôte habituelle d'Y. padellus), sont inférieures 2–3.5 fois à celles des populations de l'ensemble des autres plantes-hôtes. L'apparition de races en fonction de l'hôte, mesurée par les différences importantes dans de fréquences des allozymes entre populations sympatriques sur plusieurs plantes-hôtes, a été examinée dans quatre régions. Il apparaît ainsi que la formation de races en fonction de l'hôte se produit chez Y. padellus et que la spéciation sympatrique est un évènement très vraisemblable.