Failure of temperature to entrain a circannual rhythm of mass in California ground squirrels (Spermophilus beecheyi)

Abstract

To determine what environmental factor is the Zeitgeber for the annual change in mass, California ground squirrels (Spermophilus beecheyi) were exposed to several regimes of temperature and length of day. The squirrels were captured when age 4–5 months, kept individually in cages with excess food and nesting material. The temperature was varied with a 6‐month phase shift (SH). The length of day was the same as Santa Barbara (SB) or 6‐month phase shift (SH). The light was provided by cool white bulbs at 10–600 lux.

The first experiment consisted of keeping squirrels at either SB or SH length of day and at constant temperature (20°) for three years and then changing to SH temperature for 3 years. None entrained although at age 6, 2 might be entrained. The second experiment repeated the first except that the SH temperature started at age zero. None has entrained by age 5. None of a third group, placed at SH temperature and SB length of day, has entrained by age 3. The conclusion is that these regimes of temperature and length of day, which resemble natural conditions, do not entrain the annual change of mass.     

Donning your enemy's cloak: ground squirrels exploit rattlesnake scent to reduce predation risk

Ground squirrels (Spermophilus spp.) have evolved a battery of defences against the rattlesnakes (Crotalus spp.) that have preyed on them for millions of years. The distinctive behavioural reactions by these squirrels to rattlesnakes have recently been shown to include self-application of rattlesnake scent-squirrels apply scent by vigorously licking their fur after chewing on shed rattlesnake skins. Here, we present evidence that this behaviour is a novel antipredator defence founded on exploitation of a foreign scent. We tested three functional hypotheses for snake scent application--antipredator, conspecific deterrence and ectoparasite defence--by examining reactions to rattlesnake scent by rattlesnakes, ground squirrels and ectoparasites (fleas). Rattlesnakes were more attracted to ground squirrel scent than to ground squirrel scent mixed with rattlesnake scent or rattlesnake scent alone. However, ground squirrel behaviour and flea host choice were not affected by rattlesnake scent. Thus, ground squirrels can reduce the risk of rattlesnake predation by applying rattlesnake scent to their bodies, potentially as a form of olfactory camouflage. Opportunistic exploitation of heterospecific scents may be widespread; many species self-apply foreign odours, but few such cases have been demonstrated to serve in antipredator defence.     

Inheritance of optimal foraging behaviour in Columbian ground squirrels

Summary I examined the potential inheritance of the ability of Columbian ground squirrels (Spermophilus columbianus) to select an optimal diet. I calculated the diet that would maximize daily energy intake for each of 21 adult females and their litters, using a linear programming optimization model for each individual. The absolute value of the difference between an individual's predicted optimal diet and observed diet (deviation from an optimal diet) was used as a measure of an individual's foraging ability. The foraging ability of individuals was consistent over time and in different foraging environments, so I considered foraging ability to be a potentially heritable trait.Inheritance was determined from correlations of mother and offspring foraging ability. I experimentally removed some mothers just as they weaned their offspring so that offspring could not be influenced by their mother while learning to forage, while leaving the other mothers to raise their litters normally. In both cases, offspring strongly resembled their mother in foraging ability. However, offspring with mothers absent exhibited significantly larger deviations from their optimal diet. Offspring with mothers absent appeared to imitate their mother's diet during lactation, and this tendency partially explained their greater deviation. Consequently, offspring appear to inherit the ability to forage optimally from their mother, perhaps through observational learning or imitation. There may also be a genetic basis to foraging ability, but uncontrolled maternal effects in the experiment prevent a proper test for it.     

Individual variation in the ability of Columbian ground squirrels to select an optimal diet

Summary Columbian ground squirrels (Spermophilus columbianus) were examined for ability to select a diet that maximizes daily energy intake (optimal diet) under free-living field conditions. The optimal diet for each squirrel was determined given constraints (e.g. body size, feeding time) on individual foraging behavior. Most squirrels (63%) consumed a diet not significantly different from one that would maximize their daily energy intake. The remainder (37%) approached an energy maximized diet but appeared to make some incorrect foraging decisions. Both males and females appeared to approach energy maximized diets. An individual's deviation from its optimal diet is relatively constant within a season and not significantly affected by immediate environmental influences such as food abundance, thermal conditions and social environment. The energy cost of deviating from an optimal diet may be large enough to affect fitness. These results suggest that the ability to select an optimal diet can be viewed as a behavioral trait that might be subject to natural selection.     

The influence of hypothermia on the restoration of neural activity of brain slices from hibernating ground squirrels

1. 1. Neural activity was recorded in hippocampal slices from deep hibernating Yakut ground squirrels and in hippocampal and septal slices from non-hibernating animals.

2. 2. Slices were placed immediately after preparation in hypothermic conditions (3–4°C). Their activity was tested under standard conditions at 31°C in the incubation chamber. Some of the prepared slices were tested after maintenance in hypothermia for 2 or 24 h.

3. 3. In the hippocampal slices of hibernating ground squirrels, neural activity was present, irrespective of the period in hypothermia.

4. 4. Slices from guinea-pigs and hamsters did not possess neural activity after either 2 or 24 h of hypothermic treatment.

     

Diversity of Function of SCN Pacemakers in Behavior and Ecology of Three Species of Sciurid Rodents

Information on the widespread function of the suprachiasmatic (SCN) pacemaker has increased dramatically in the past decade for laboratory rodents and for humans. Interest is now also growing in the adaptive value of SCN pacemakers in wild species of free-living mammals in natural pristine habitat. The squirrel family, Sciuridae, is highly diverse in North America. Radiation into many specialized groups has evolved in response to the temporal and spatial characteristics of specific habitats. The sciurids thus offer possibilities for comparison of SCN function for closely related species from very different habitats. Results from field and laboratory investigations concerning the ecological significance of the SCN are reported here for three ground squirrel species. The semi-fossorial antelope squirrels of the American southwest deserts were arrhythmic in above ground activities after deletion of the SCN pacemaker. In a desert enclosure, predation rates rose dramatically for lesioned animals in comparison to intact controls. The semi-arborial chipmunks were prone to capture by mustelid burrow predators such as weasels after SCN-deletion, even though the chipmunks did not exhibit any above ground activity at night. The telltale cue for the predator was apparently arrhythmic restlessness within the complex home burrow. The semi-fossorial golden-mantled squirrels of the Cascade Mountains of western United States rely on profound, long-lasting hibernation for over-wintering. Periods of torpor alternate with brief euthermic arousal episodes lasting less than 24 h throughout the 5- to 8-month winter phase. Deletion of the SCN in golden-mantled squirrels resulted in aberrations of hibernation arousal patterns that were metabolically expensive and put individuals at risk of starvation immediately after emergence in spring.     

Territoriality and male reproductive success in arctic ground squirrels

Although territorial defense is a common form of reproductivecompetition among male vertebrates, the exact reproductiveconsequences of this behavior are often poorly understood.To explore relationships between territoriality and reproductivesuccess in a nongroup-living mammal, we quantified patterns of space use, mating success, and fertilization success formales in a free-living population of arctic ground squirrels(Spermophilus parryii plesius). Because litters of this speciesare sired almost exclusively by a female's first mate, we predictedthat territory ownership would be associated with first accessto estrous females. During the 2-week period when mating occurred,each male in the study population attempted to defend a distinctportion of the habitat, although the success of this defensevaried among individuals. Twenty-six of 28 females monitoredmated with the male on whose territory they resided. However,the majority of females observed throughout estrus (65%; n= 20) also mated with at least one other male, indicating thatterritory ownership was not associated with exclusive accessto females. In contrast, territory ownership was significantly associated with first access to estrous females; 20 (71.4%)of 28 females mated first with the male on whose territorythey resided. In this regard, the behavior of S. parryii plesiusparallels that of socially monogamous birds in which territorialdefense by males functions to deter extrapair copulations byfemales. Although territorial defense represents an important component of male reproductive success in arctic ground squirrels,other aspects of male behavior (e.g., the ability to dominateagonistic interactions on the day of a female's estrus) arealso critical. We suggest that future studies of vertebratemating systems will benefit by viewing such defense as onlyone of multiple axes along which conspecific males compete foraccess to females.     

达乌尔黄鼠犁鼻器和副嗅球的组织结构及嗅球c-Fos表达的季节变化

啮齿动物的犁鼻器和副嗅球与社会通讯和生殖行为有关,主嗅球影响其觅食行为。达乌尔黄鼠（Spermophilus dauricus）是一种具有较低社会行为的储脂类冬眠动物。本研究用组织学和免疫组织化学方法探究了其犁鼻器和副嗅球的结构特点及嗅球神经元活动对季节变化的适应。结果发现,达乌尔黄鼠犁鼻器具有较大的血管,犁鼻器管腔外侧为非感觉性的呼吸上皮（Respiratory epithelium,RE）,内侧为感觉上皮（Sensory epithelium,SE）,RE较SE薄,靠近管腔处为假复层柱状上皮。选取犁鼻器中间部位比较,发现SE的厚度、长度及感觉细胞密度均无性别差异。副嗅球位于主嗅球后方背内侧,由6层细胞构成。侧嗅束穿过副嗅球,位于颗粒细胞层之上。雄性达乌尔黄鼠较雌性有更长的僧帽细胞层和颗粒细胞层。春季（3月）和冬季（1月）达乌尔黄鼠主嗅球的嗅小球层、僧帽细胞层和颗粒细胞层的c-Fos-ir神经元密度显著低于夏季（7月）和秋季（10月）,且冬季外网织层的c-Fos-ir神经元密度显著低于夏季和秋季,说明达乌尔黄鼠在冬季和春季的嗅觉神经活动较弱,呈现出对冬眠的生理性适应。这些结果丰富了动物犁鼻器和副嗅球的形态学资料,并有助于理解冬眠动物嗅觉系统对季节变化和冬眠的适应。     

Changes in the pollen seasons of the early flowering trees <Emphasis Type=Italic>Alnus</Emphasis> spp. and <Emphasis Type=Italic>Corylus</Emphasis> spp. in Worcester,United Kingdom, 1996–2005

Previous work on Betula spp. (birch) in the UK and at five sites in Europe has shown that pollen seasons for this taxon have tended to become earlier by about 5–10 days per decade in most regions investigated over the last 30 years. This pattern has been linked to the trend to warmer winters and springs in recent years. However, little work has been done to investigate the changes in the pollen seasons for the early flowering trees. Several of these, such as Alnus spp. and Corylus spp., have allergens, which cross-react with those of Betula spp., and so have a priming effect on allergic people. This paper investigates pollen seasons for Alnus spp. and Corylus spp. for the years 1996–2005 at Worcester, in the West Midlands, United Kingdom. Pollen data for daily average counts were collected using a Burkard volumetric trap sited on the exposed roof of a three-storey building. The climate is western maritime. Meteorological data for daily temperatures (maximum and minimum) and rainfall were obtained from the local monitoring sites. The local area up to approximately 10 km surrounding the site is mostly level terrain with some undulating hills and valleys. The local vegetation is mixed farmland and deciduous woodland. The pollen seasons for the two taxa investigated are typically late December or early January to late March. Various ways of defining the start and end of the pollen seasons were considered for these taxa, but the most useful was the 1% method whereby the season is deemed to have started when 1% of the total catch is achieved and to have ended when 99% is reached. The cumulative catches (in grains/m³) for Alnus spp. varied from 698 (2001) to 3,467 (2004). For Corylus spp., they varied from 65 (2001) to 4,933 (2004). The start dates for Alnus spp. showed 39 days difference in the 10 years (earliest 2000 day 21, latest 1996 day 60). The end dates differed by 26 days and the length of season differed by 15 days. The last 4 years in the set had notably higher cumulative counts than the first 2, but there was no trend towards earlier starts. For Corylus spp. start days also differed by 39 days (earliest 1999 day 5, latest 1996 day 44). The end date differed by 35 days and length of season by 26 days. Cumulative counts and lengths of season showed a distinct pattern of alternative high (long) and low (short) years. There is some evidence of a synchronous pattern for Alnus spp.. These patterns show some significant correlations with temperature and rainfall through the autumn, winter and early spring, and some relationships with growth degree 4s and chill units, but the series is too short to discern trends. The analysis has provided insight to the variation in the seasons for these early flowering trees and will form a basis for future work on building predictive models for these taxa.     

Growth and Differentiation of Adult Hippocampal Arctic Ground Squirrel Neural Stem Cells

Arctic ground squirrels (Urocitellus parryii, AGS) are unique in their ability to hibernate with a core body temperature near or below freezing ¹. These animals also resist ischemic injury to the brain in vivo^2,3 and oxygen-glucose deprivation in vitro^4,5. These unique qualities provided the impetus to isolate AGS neurons to examine inherent neuronal characteristics that could account for the capacity of AGS neurons to resist injury and cell death caused by ischemia and extremely cold temperatures. Identifying proteins or gene targets that allow for the distinctive properties of these cells could aid in the discovery of effective therapies for a number of ischemic indications and for the study of cold tolerance. Adult AGS hippocampus contains neural stem cells that continue to proliferate, allowing for easy expansion of these stem cells in culture. We describe here methods by which researchers can utilize these stem cells and differentiated neurons for any number of purposes. By closely following these steps the AGS neural stem cells can be expanded through two passages or more and then differentiated to a culture high in TUJ1-positive neurons (~50%) without utilizing toxic chemicals to minimize the number of dividing cells. Ischemia induces neurogenesis ⁶ and neurogenesis which proceeds via MEK/ERK and PI3K/Akt survival signaling pathways contributes to ischemia resistance in vivo⁷ and in vitro⁸ (Kelleher-Anderson, Drew et al., in preparation). Further characterization of these unique neural cells can advance on many fronts, using some or all of these methods.     

Genetic diversity and population divergence in fragmented habitats: Conservation of Idaho ground squirrels

The Idaho ground squirrel, which consists of a northern (Spermophilus brunneus brunneus) and a southern subspecies (S. b. endemicus), has suffered from habitat loss and fragmentation, resulting in a reduction in both numbers and geographic range of the species. The northern Idaho ground squirrel (NIDGS) is listed as a threatened subspecies under the Endangered Species Act, and the southern Idaho ground squirrel (SIDGS) is a candidate. Because Idaho ground squirrel populations are small and often isolated, they are susceptible to inbreeding and loss of genetic diversity through drift. This research evaluates levels of genetic diversity and patterns of population divergence in both subspecies of Idaho ground squirrels. We hypothesized that NIDGS would exhibit lower genetic diversity and greater population divergence due to a longer period of population isolation relative to most SIDGS populations. Genetic diversity and divergence were quantified using 8 microsatellite loci. Contrary to expectations, SIDGS populations exhibited consistently lower levels of microsatellite diversity. Additionally, NIDGS exhibited only modest divergence among populations, while divergence levels among SIDGS populations were highly varied. Preliminary evaluations of mitochondrial DNA diversity and structure revealed lower diversity in NIDGS and some differences in gene flow that warrant further study. Based on our results, we suggest different management strategies for the two subspecies. Habitat restoration appears to be the most desirable conservation strategy for NIDGS populations. In contrast, low genetic diversity observed in SIDGS may warrant supplementation of isolated populations through translocations or captive breeding to mitigate further loss of genetic variability.     

Suppression of MAPKAPK2 during mammalian hibernation

Metabolic signaling coordinates the transition by hibernating mammals from euthermia into profound torpor. Organ-specific responses by activated p38 mitogen activated protein kinase (MAPK) are known to contribute to this transition. Therefore, we hypothesized that the MAPK-activated protein kinase-2 (MAPKAPK2), a downstream target of p38 MAPK, would also be active in establishing the torpid state. Kinetic parameters of MAPKAPK2 from skeletal muscle of Richardson’s ground squirrels, Spermophilus richardsonii, were analyzed using a fluorescence assay. MAPKAPK2 activity was 27.4 ± 1.27 pmol/min/mg in muscle from euthermic squirrels and decreased by ∼63% during cold torpor, while total protein levels were unchanged (as assessed by immunoblotting). In vitro treatment of MAPKAPK2 via stimulation of endogenous phosphatases and addition of commercial alkaline phosphatase decreased enzyme activity to only ∼3–5% of its original value in muscle extracts from both euthermic and hibernating squirrels suggesting that posttranslational modification suppresses MAPKAPK2 during the transition from euthermic to torpid states. Enzyme S_0.5 and n_H values for ATP and peptide substrates changed significantly between euthermia and torpor, and also between assays at 22 versus 10 °C but, kinetic parameters were actually closely conserved when values for the euthermic enzyme at 22 °C were directly compared with the hibernator enzyme at 10 °C. Arrhenius plots showed significantly different activation energies of 40.8 ± 0.7 and 54.3 ± 2.7 kJ/mol for the muscle enzyme from euthermic versus torpid animals, respectively but MAPKAPK2 from the two physiological states showed no difference in sensitivity to urea denaturation. Overall, the results show that total activity of MAPKAPK2 is in fact reduced, despite previous findings of p38 MAPK activation, and kinetic parameters are altered when ground squirrels enter torpor but protein stability is not apparently changed. The data suggest that MAPKAPK2 suppression may have a significant role in the differential regulation of muscle target proteins when ground squirrels enter torpor.     

Fire and ice: genetic structure of the Uinta ground squirrel (Spermophilus armatus) across the Yellowstone hotspot

The range of the Uinta ground squirrel, Spermophilus armatus , is centred over one of the most tectonically active regions today, the Yellowstone hotspot. We document the role of Quaternary tectonic and climatic history on the genetic structure of this species by screening museum and extant individuals throughout its range. Phylogeographic, divergence time, and demographic analyses of partial mitochondrial cytochrome b and control region DNA sequences yield insight into the cadence of evolution across three spatiotemporal scales: (i) a relatively deep intraspecific divergence of S. armatus into three lineages coincident with the last major volcanic eruption in the region and maintained by the Snake River Plain; (ii) demographic expansion in two lineages corresponding to the time of last deglaciation of the region; and (iii) a recent (< 50 years) local extinction of the third lineage coincident with climatic change and conversion of habitat for agricultural purposes in eastern Idaho. Beyond these inferences, our study highlights the unique value of museum material to phylogeography, and shows that small mammal recolonization of previously glaciated montane 'islands' differs from northward postglacial expansion observed in areas previously covered by continental ice sheets. Montane 'islands' may harbour high genetic diversity because of admixture and recurrent expansion/extinction.