Features of Interspecific Contacts and Hybridization of Ground Squirrels (Marmotinae,Sciuridae, Rodentia) in Mongolia

Using molecular genetic methods, we investigated the secondary contact zones of two pairs of species of ground squirrels of Mongolia. In common colonies of marmots M. sibirica and M. baibacina, we revealed a high frequency of occurrence of hybrid individuals that were viable and fertile. A hybridization between S. alaschanicus and S. pallidicauda was sporadic in nature. The hypothesis about an extensive hybrid zone in these species of ground squirrels was not confirmed. An occupation of suboptimal biotopes by individuals of different species was the main factor contributing to hybridization in both case. The complex social behavior in marmots affected on the localization and diffusion of the hybridization process.     

A Molecular Genetic Study of Hybridization in Four Species of Ground Squirrels (Spermophilus: Rodentia,Sciuridae)

Four species of ground squirrel—yellow (Spermophilus fulvus), russet (S. major), small (S. pygmaeus), and spotted (S. suslicus)—occur in the Volga region. Between S. major and S. pigmaeus, S. major and S. fulvus, and S. major and S. suslicus, sporadic hybridization was reported. Using sequencing and restriction analysis, we have examined the mtDNA C region in 13 yellow, 60 russet, 61 small, 45 spotted ground squirrels, and 9 phenotypic hybrids between these species. It was shown that 43% of S. major individuals had alien mitotypes typical of S. fulvus and S. pygmaeus. Alien mitotypes occurred both within and outside sympatric zones. No alien mitotypes were found in 119 animals of the other three species, which suggests that only one parental species (S. major) predominantly participates in backcrosses. Phenotypic hybrids S. fulvus × S. major and S. major × S. pygmaeus) were reliably identified using RAPD–PCR of nuclear DNA. However, we could find no significant traces of hybridization in S. major with alien mitotypes. Analysis of p53 pseudogenes of S. major and S. fulvus that were for the first time described in the present study produced similar results: 59 out of 60 individuals of S. major (including S. major with S. fulvus mitotypes) had only the pseudogene variant specific for S. major. This situation is possible even at low hybridization frequencies (less than 1% according to field observations and 1.4 to 2.7% according to nuclear DNA analysis) if dispersal of S. major from the sympatric zones mainly involved animals that obtained alien mtDNA via backcrossing. The prevalence of animals with alien mitotypes in some S. major populations can be explained by the founder effect. Further studies based on large samples are required for clarifying the discrepancies between mitochondrial and nuclear DNA data.     

Comparative Ontogeny of Behaviour in Four Species of Squirrels (Sciuridae)

The development of behaviour in four species of Sciurid rodents, having terrestrial, arboreal and gliding way of life, is quantified and compared. The studied species are: Spermophilus columbianus, Spermophilus lateralis, Tamiasciurus hudsonicus and Glaucomys sabrinus. For each behaviour pattern, the earliest and latest age of emergence is given along with a mean calculated for a series of young of each species. The development of locomotion, feeding, comfort, alertness, exploration, nest building and social behaviour and the principal events of physical development are analysed. The discussion shows that the specific differences in ontogenetic rate are controlled by a series of factors including predation pressure, hibernation and the specific complexity of locomotion.     

Probing,Assessment and Management during Interactions between Ground Squirrels (Rodentia: Sciuridae) and Rattlesnakes (Squamata: Viperidae). 2: Cues Afforded by Rattlesnake Rattling

The predator-prey relationship between California ground squirrels (Spermophilus beecheyi) and northern Pacific rattlesnakes (Crotalus riridis oreganus) is a useful system in which to explore risk assessment and management. Rattlesnakes are major predators of ground-squirrel pups, but pose only a sublethal threat to adult squirrels. Adults approach, harass, and even attack rattlesnakes when confronted with them. A rattlesnake's response to such harassment can include rattling and striking. Not all rattlesnakes pose the same risk to an adult squirrel. Larger, warmer rattlesnakes strike in ways that may be more effective at overwhelming the defensive leaps of squirrels, and larger snakes can inject more venom if they are successful in landing a bite. It would therefore benefit squirrels to assess and respond appropriately to rattlesnakes of different body size and temperature. We looked for cues in rattling upon which such assessments might be based. We recorded and digitally analyzed the rattling sounds of snakes of different sizes, each tested at four different body temperatures — 10, 18, 27, and 35°C. Results indicate that warmer snakes rattle with faster click rates, higher amplitudes, and shorter latencies. Similarly, larger snakes produce rattling sounds of higher amplitude and lower dominant frequencies. Thus, rattling provides reliable cues about rattlesnake dangerousness. Nevertheless, this highly ‘informative’ characteristic of rattling has its origins in physical and physiological constraints, not in specialization for communication. Ground squirrels appear to probe for the information extractable from rattling, for example by pushing loose substrate at the snake and thus inducing it to rattle. Future reports will discuss the degree to which ground squirrels actually exploit these cues.     

Historical Biogeography and Body Form Evolution of Ground Squirrels (Sciuridae: Xerinae)

Xerinae is the most species-rich subfamily of the Sciuridae (Rodentia). This group of animals has a long complex evolutionary history, which witnessed severe environmental changes. In this paper, a comprehensive approach integrating information from fossil records, morphological, molecular and geographical data of extant species, and events of paleoclimate and paleogeography, were used to explore the evolutionary processes in the Xerinae. Xerinae probably originated in Eurasia around the early Oligocene, and dispersed to Africa via the Africa-Eurasia Land Bridge on two occasions during the Miocene, and subsequently evolved into the Protoxerini and African Xerini. The tribe Marmotini derived from a Eurasian ancestor and thrived in North America. Tamias re-occupied Eurasia in the early Miocene, while the distributions of Marmota and ‘Spermophilus’ genus-groups were restricted to North America at least until the late Miocene. Global cooling and the emergence of grass-dominated ecosystems from 15 Ma are likely to be the main causes for the radiation of Marmotini. The body form of Xerinae displays an allometric mode of evolution, with ground-living taxa, such as Marmota, Cynomys and Xerus notably enlarged, while Tamias has remained slim in body form. To cope with the global environmental changes, particularly the global cooling induced forest degradation and grassland expansion in the late Miocene, most Marmotini developed into true ground squirrels with short tails. The slim body adaptation in Tamias may be related to competition from tree squirrels, or their hoarding behavior, the latter helping them to cope with cold winter.     

Plasticity of Alarm-call Response Development in Belding's Ground Squirrels (Spermophilus beldingi, Sciuridae)

Plasticity in the alarm-call responses of Belding's ground squirrels ( Spermophilus beldingi ) may function to prepare young to respond appropriately to calls according to the predator environment and habitat in which the young develop. To examine the extent to which antipredator responses are sensitive to early rearing environments, we studied the development of behavioural responses to playbacks of alarm calls and non-alarm calls in free-living juveniles and captive juveniles housed in large outdoor enclosures. Compared with same-aged, free-living juveniles, captive juveniles were more likely to show an observable response to playbacks, exhibited more exaggerated initial responses (e.g. enter a burrow vs. freeze), and remained alert longer following playbacks. The influence of rearing history on antipredator responses was limited to responses to auditory stimuli, as the two groups of juveniles reacted similarly to fast-moving visual stimuli. The responses of free-living juveniles appeared to be more discriminating than responses of captive juveniles, particularly following playbacks of calls associated with less immediate threats.
The responses of captive and free-living mothers were similar, indicating a developmental component to the juvenile response differences observed here. Free-living juveniles developed a discrimination among alarm and non-alarm calls sooner than captive young. Response differences were evident within 1 wk of first emergence from natal burrows and persisted at least 4 wk, at around the age of natal dispersal. This suggests that early rearing history has an enduring effect on response repertoires, which may be adaptive if animals continue to inhabit the predator environment in which they developed.     

Foraging behaviour of the Brazilian squirrelSciurus aestuans (Rodentia, Sciuridae)

We describe the foraging behaviour of the Brazilian squirrelSciurus aestuans Linnaeus, 1776 in a natural free-living population, in an area with a high concentration of palm fruitsSyagrus romanzoffiana (Chamisso) Glassman. Our objective was to investigate if the abundance ofS. romanzoffiana fruits, an important food item for squirrels, temporally influenced the foraging behaviour of this population. The observations were carried out over an eight-month (April–November 2001) period. Fruiting phenology ofS. romanzoffiana was also monitored. The most consumed food item for this period was the fruit ofS. romanzoffiana (70%), followed by foods of human origin (14%). The percentage of time spent feeding increased in September, and the time spent travelling declined in September, October and November, when females were observed showing evidence of reproductive activity. At the same timeS. romanzoffiana fruits become available. The consumption of human items illustrates the opportunistic feeding habit of these squirrels, but variations in foraging behaviour detected probably were more strongly related to availability ofS. romanzoffiana fruits.     

Phylogeny and Evolutionary History of the Ground Squirrels (Rodentia: Marmotinae)

Although ground squirrels (Spermophilus) and prairie dogs (Cynomys) are among the most intensively studied groups of mammals with respect to their ecology and behavior, a well-resolved phylogeny has not been available to provide a framework for comparative and historical analyses. We used complete mitochondrial cytochrome b sequences to construct a phylogeny that includes all 43 currently recognized species in the two genera, as well as representatives of two closely related genera (Marmota and Ammospermophilus). In addition, divergence times for ground squirrel lineages were estimated using Bayesian techniques that do not assume a molecular clock. All methods of phylogenetic analysis recovered the same major clades, and showed the genus Spermophilus to be paraphyletic with respect to both Marmota and Cynomys. Not only is the phylogeny at odds with previous hypotheses of ground squirrel relationships, but it suggests that convergence in morphology has been a common theme in ground squirrel evolution. A well-supported basal clade, including Ammospermophilus and two species in the subgenus Otospermophilus, diverged from all other ground squirrels an estimated 17.5 million years ago. Between 10 and 14 million years ago, a relatively rapid diversification gave rise to lineages leading to marmots and to several distinct groups of ground squirrels. The Eurasian ground squirrels diverged from their North American relatives during this period, far earlier than previously hypothesized. This period of diversification corresponded to warming climate and spread of grasslands in western North America and Eurasia. Close geographic proximity of related forms suggests that most species evolved in or near their current ranges.     

Blood and intestinal parasites of squirrels (Rodentia: Sciuridae) in Amazonian Brazil

We report the result of an examination for blood and intestinal protozoa in 12 specimens of the red squirrel Sciurus spadiceus (Rodentia: Sciuridae) from Birroque, municipality of Placido de Castro, state of Acre, Brazil. No parasites were detected in thin, Giemsa-stained blood films of the animals, but culture of the blood of three in Difco B45 medium blood-agar slants gave rise to isolates of epimastigotes. Inoculation of one isolate into laboratory mice resulted in the appearance of Trypanosoma cruzi-like trypomastigotes in their peripheral blood, and the other two isolates gave rise to transient infections with a T. lewisi-like parasite in inoculated mice and hamsters. The failure of the latter parasite to develop in the triatomine bug Rhodnius robustus suggests that it is probably not T. rangeli. This appears to be the first record of a T. lewisi-like trypanosome in neotropical squirrels. Oocysts of an Eimeria sp., were detected in the faeces of 10 animals (83.3%). The parasite develops in the epithelial cells of the intestine, where it may cause severe damage and sometimes results in death of the animal. No oocysts were detected in bile.     

Alarm Calls Affect Foraging Behavior in Eastern Chipmunks (Tamias striatus, Rodentia: Sciuridae)

We used playback experiments to test whether alarm calls affected the foraging behavior of eastern chipmunks (Tamias striatus). We subjected chipmunks, foraging at artificial feeding stations, to three playback treatments (silent, control noise, and alarm call) and examined changes in vigilant and foraging behavior. Chipmunks responded to alarm calls with a greater degree and duration of vigilant behavior, such as look‐ups and alert postures. Chipmunks also ran a shorter distance to cover and took longer to re‐emerge from the burrow after hearing an alarm call. Alarm calls caused individuals to spend more time exposed at the feeding stations; however, individuals also took significantly fewer seeds after hearing an alarm call. This was not due to a difference in the time spent handling food, but rather to a slower rate of loading. Chipmunks appear to sacrifice energy gain by increasing vigilance after hearing an alarm call. This study suggests that to avoid the costs of unnecessary escape behavior, individuals directly assess their own risk rather than relying only on indirect cues such as alarm calls.     

How Rearing History Affects Alarm-call Responses of Belding's Ground Squirrels (Spermophilus beldingi, Sciuridae)

Juvenile, but not adult, Belding’s ground squirrels (Spermophilus beldingi) exhibit markedly different responses to alarm calls as a function of their environment. Compared with same-aged, free-living juveniles, captive juveniles (housed in large outdoor enclosures) are more likely to respond to playbacks, to exhibit more exaggerated initial responses (e.g. enter a burrow vs. freeze) and to remain alert longer following playbacks of alarm and non-alarm calls. Two studies were conducted to identify the factors contributing to these response differences. Postemergent rearing environments (such as the opaque enclosure walls that limited visual and auditory stimulation in captivity, or the increased number of conspecifics and natural alarm calls that free-living juveniles experienced) could not account for the majority of response differences between captive and free-living juveniles (Study 1). To determine if the attenuated responses of free-living juveniles were due to foraging pressures, we compared the behaviours of food-provisioned captive juveniles with those of non-provisioned captive juveniles. Although sample sizes were small, no differences were evident in the development or expression of responses as a function of foraging pressure. Next, the development of captive juveniles was compared with that of juveniles reared in the field but housed in captivity after emergence (Study 2). Differences in the response patterns of field-reared and captive-reared animals matched the differences reported previously, as the responses of field-reared animals observed in captivity mirrored those of free-living juveniles that remained in the field. Thus, the differences in alarm-call responses originally observed between captive and free-living juveniles are attributed to their pre-emergent, but not post-emergent, rearing histories. Captive pups experienced levels of auditory, visual, tactile, and olfactory stimulation that were greater than those typically experienced by free-living pups. The increased exposure to conspecific alarm calls may have primed captive pups to respond more often and more intensely to the auditory stimuli they heard as juveniles. Sensitivity to early rearing environments may be adaptive for young ground squirrels if it facilitates the development of antipredator behaviour patterns that are appropriate for the local predator environment (e.g. openness of habitat, frequency of predators, availability of refuges).     

Information and Patch Exploitation Strategies of the Eastern Chipmunk,Tamias striatus (Rodentia: Sciuridae)

We examined to what extent 15 chipmunks foraging from dishes in the field varied load sizes depending on a predetermined sequence of resource renewal/removal. At 10-m distances from burrows, chipmunks collected smaller loads when seeds were replenished over sequential trials and larger load sizes when trials were interrupted by removing all seeds for one visit. Similar sequence effects were less obvious at 0 m. Load size also varied with travel time but not in a manner consistent with either long-term rate maximization or resource tracking. When travel time effects were removed, sequence effects became more pronounced at distances of both 0 and 10 m. The results suggest that chipmunks use past experience in patches to gauge expected returns in the future, and that they devalue resources according to their uncertainty (“future discounting”). That chipmunks varied load sizes with food renewal/removal more at 10 than 0 m from burrows suggests that the degree to which chipmunks devalue future resources may depend on how defendable those resources are.     

Serum thyroxine and seasonal fattening of free-living Piute ground squirrels, Spermophilus mollis (Rodentia: Sciuridae)

Serum thyroxine and body composition of free-living Piute ground squirrels were examined during the season of above-ground activity. Serum thyroxine titers were 2-10 times higher than those reported in laboratory studies on other species. Among juveniles, both body size and lipid content were negatively correlated with thyroxine, whereas these variables were not significantly correlated among adults. Significant sex differences in serum thyroxine were observed for both age groups. Results suggest that the seasonal cycle of body weight is driven by an underlying metabolic cycle but that individual fattening schedules are determined by environmental conditions.     

水松生物学特性及保护(综述)

本文全面地综述水松的外部形态特征和内部结构,其内部结构包括苗端、叶片、树皮、木材结构、雌雄配子体和胚胎发育、花粉和染色体。此外,还概述水松的地理分布、生态学与群落学特征。初步分析水松的濒危原因,提出具体保护措施。     

A new species of Sciurodendrium (Nematoda: Heligmonellidae) in Sciurus aureogaster (Rodentia: Sciuridae) from Morelos, Mexico

Sciurodendrium bravohollisae n. sp. (Heligmonellidae) is described as an intestinal parasite of 2 squirrels, Sciurus aureogaster Cuvier, 1829, collected from Los Robles, Municipio de Tlalnepantla, Morelos State, Mexico. The new species differs from all other congeners in possessing a very well-developed and sacciform genital cone. This is the seventh species described for the genus and the first one recorded in Mexico.     

Molecular phylogeny of the marmots (Rodentia: Sciuridae): tests of evolutionary and biogeographic hypotheses

There are 14 species of marmots distributed across the Holarctic, and despite extensive systematic study, their phylogenetic relationships remain largely unresolved. In particular, comprehensive studies have been lacking. A well-supported phylogeny is needed to place the numerous ecological and behavioral studies on marmots in an evolutionary context. To address this situation, we obtained complete cytochrome (cyt) b sequences for 13 of the species and a partial sequence for the 14th. We applied a statistical approach to both phylogeny estimation and hypothesis testing, using parsimony and maximum likelihood-based methods. We conducted statistical tests on a suite of previously proposed hypotheses of phylogenetic relationships and biogeographic histories. The cyt b data strongly support the monophyly of Marmota and a western montane clade in the Nearctic. Although some other scenarios cannot be rejected, the results are consistent with an initial diversification in North America, followed by an invasion and subsequent rapid diversification in the Palearctic. These analyses reject the two major competing hypotheses of M. broweri's phylogenetic relationships--namely, that it is the sister species to M. camtschatica of eastern Siberia, and that it is related closely to M. caligata of the Nearctic. The Alaskan distribution of M. broweri is best explained as a reinvasion from the Palearctic, but a Nearctic origin can not be rejected. Several other conventionally recognized species groups can also be rejected. Social evolution has been homoplastic, with large colonial systems evolving in two groups convergently. The cyt b data do not provide unambiguous resolution of several basal nodes in the Palearctic radiation, leaving some aspects of pelage and karyotypic evolution equivocal.     

Feeding habits of the squirrel Sciurus variegatoides (Rodentia: Sciuridae) in the Nicoya Peninsula, Costa Rica

Food items consumed by the squirrel Sciurus variegatoides atrirufus were determined in an agricultural setting in the Nicoya Peninsula (9 degrees 47' N, 84 degrees 56' W), Costa Rica, where two life zones (Premontane Moist Forest Basal Belt Transition, and Tropical Dry Forest) predominate. By analyzing the gut contents of 120 squirrels, from February 1987 through January 1988, it was determined that coconut (Cocos nucifera), indian almond (Terminalia catappa) and flamboyant (Delonix regia) were the most common dietary items. There were differences in food consumption according to age: adults preferred coconut, whereas young individuals preferred almond. This finding can be explained in terms of fruit characteristics, as well as tree architecture and accessibility for squirrels; almendro trees provide higher protection and a more accessible food resource, so that it was better used by young individuals.