Seasonal shedding of multiple Cryptosporidium genotypes in California ground squirrels (Spermophilus beecheyi)

Twelve percent of 853 California ground squirrels (Spermophilus beecheyi) from six different geographic locations in Kern County, Calif., were found to be shedding on average 44,482 oocysts g of feces(-1). The mean annual environmental loading rate of Cryptosporidium oocysts was 57,882 oocysts squirrel(-1) day(-1), with seasonal patterns of fecal shedding ranging from <10,000 oocysts squirrel(-1) day(-1) in fall, winter, and spring to levels of 2 x 10(5) oocysts squirrel(-1) day(-1) in summer. Juveniles were about twice as likely as adult squirrels to be infected and shed higher concentrations of oocysts than adults did, with particularly high levels of infection and shedding being found among juvenile male squirrels. Based on DNA sequencing of a portion of the 18S small-subunit rRNA gene, there existed three genotypes of Cryptosporidium species in these populations of squirrels (Sbey03a, Sbey03b, and Sbey03c; accession numbers AY462231 to AY462233, respectively). These unique DNA sequences were most closely related (96 to 97% homology) to porcine C. parvum (AF115377) and C. wrairi (AF115378). Inoculating BALB/c neonatal mice with up to 10,000 Sbey03b or Sbey03c fresh oocysts from different infected hosts did not produce detectable levels of infection, suggesting that this common genotype shed by California ground squirrels is not infectious for mice and may constitute a new species of Cryptosporidium.     

Genetic evidence of extensive introgression of short-tailed ground squirrel genes in a hybridization zone of Spermophilus major and S. erythrogenys, inferred from sequencing of the mtDNA cytochrome b gene

We have completely sequenced the mtDNA cytochrome b gene of ground squirrels from the zone of overlapping ranges of Spermophilus major and S. erythrogenys in the Tobol-Ishim interfluve, which is a putative hybridization zone of these species. The results of the sequencing showed extensive introgression of mtDNA genes of the short-tailed ground squirrel S. e. brevicauda, whose haplotype had fully replaced the S. major haplotype. All of the ground squirrels from the Tobol-Ishim interfluve had a variant of the S. e. brevicauda mtDNA haplotype that was specific for this zone. On average, 119 substitutions (10.44%) were found between S. major from Ul'yanovsk oblast and S. e. brevicauda from the northern Kazakhstan, the mean genetic distance (D) between them being 0.115, which conforms to the corresponding parameters for the S. e. brevicauda-S. pygmaeus pair (122 substitutions, D = 118). Insignificant differences (seven substitutions, D = 0.043) were found between the S. major and S. pygmaeus haplotypes, which suggest that these species have similar mitochondrial haplotypes. Five to ten nucleotide substitutions (0.44--0.88%) were detected between the animals from the Tobol--Ishim interfluve and S. e. brevicauda. The mtDNA haplotype divergence D within the genus Spermophilus (ten species) for all codon positions ranged from 0.035 to 0.158. Phylogenetic reconstructions (MP, ML, and NJ trees) showed two well-differentiated clusters with high bootstrap support. However, there was different branching topology within the cluster and their species composition varied. The maximum likelihood tree, ML, differentiating the species into two subgenera, Citellus and Colobotis, most reliably reflected taxonomic relationships of the species from the genus Spermophilus, inferred from morphological and genetic biochemical data. The morphologically pure S. major (subgenus Colobotis) animals, used in the analysis, proved to carry the haplotype of another species, S. pygmaeus (subgenus Citellus). This poses a question on the existence of the specific haplotype of S. major, the reason of its replacement by haplotype of other species, and possible consequences of this phenomenon for survival of the species.     

Genetic evidence of hybridization between paletailed Spermophilus pallidicauda Satunin, 1903 and alashanic S. alaschanicus Buchner, 1888 ground squirrels in Mongolia

Analysis of Spermophilus pallidicauda Satunin, 1903 from three localities in Mongolia using cytogenetic characteristics (chromosome number and morphology, as well as the number and localization of nucleolus organizer regions) revealed the presence of a first-generation (F1) hybrid animal (2n = 36), of the paletailed S. pallidicauda (2n = 34) and alashanic S. alaschanicus (2n = 38) ground squirrels in the contact zone of their ranges. Analysis of nuclear DNA from ten ground squirrels (from a set of karyologically examined animals) by RAPD-PCR with eight oligonucleotide primers (OPA10, OPA12, OPC02, OPC5, OPC08, OPC09, OPC12, and OPD05) revealed four hybrids in two sites. with one of the hybrid being F1. The position of the hybrids in phylogenetic reconstructions made for the subgenera Citellus and Colobotis species varied depending on the method used. In the UPGMA dendrogram of genetic similarity hybrids formed their own subcluster with high bootstrap index (949) within the cluster of Citellus species. In the NJ phylogenetic tree, hybrids also clustered with high boot-strap index (886). But in this case they were located between the Colobotis and Citellus species clusters. The mtDNA haplotypes of the three hybrids examined were highly similar to the Colobotis ground squirrels, albeit in phylogenetic reconstructions they were placed between Colobotis and Citellus. The sites of the hybrid animals identification were located more than 200 km apart. Hence, the contact zone between the S. pallidicauda and S. alaschanicus can encompass a large territory in Mongolia.     

Quantitative shedding of two genotypes of Cryptosporidium parvum in California ground squirrels (Spermophilus beecheyi)

Sixteen percent of California ground squirrels (Spermophilus beecheyi) were found to be shedding an average of 53,875 Cryptosporidium parvum oocysts/g of feces. Male squirrels had a higher prevalence and higher intensity of shedding than did female squirrels. The majority of C. parvum isolates matched a bovine-murine genotype, with a few isolates resembling a porcine genotype. Higher intensities of shedding by males may enhance dissemination and genotypic mixing of this protozoa given males' proclivity to disperse to nonnatal colonies.     

Host usage and seasonal activity patterns of Ixodes kingi and I. sculptus (Acari: Ixodidae) nymphs in a Colorado prairie landscape, with a summary of published North American host records for all life stages.

We examined host usage and seasonal activity patterns of the nymphal stage of the ticks Ixodes kingi and I. sculptus within a prairie rodent community in north-central Colorado. Ixodes kingi was commonly encountered on both northern grasshopper mice (Onychomys leucogaster) and thirteen-lined ground squirrels (Spermophilus tridecemlineatus), whereas I. sculptus frequently infested S. tridecemlineatus but was absent from O. leucogaster. Low numbers of ticks of both species were collected from deer mice (Peromyscus maniculatus) and Ord's kangaroo rats (Dipodomys ordii). Nymphal loads of I. kingi and I. sculptus increased dramatically on commonly infested rodent species from spring (May-June) to summer (July-August). Further, rodents trapped on prairie-dog towns tended to experience increased nymphal loads of I. kingi (O. leucogaster, S. tridecemlineatus) but decreased loads of I. sculptus (S. tridecemlineatus) following plague epizootics among prairie dog populations. A summary of published North American host records revealed that I. kingi has been recorded from humans, domestic animals (cat, dog), 17 species of carnivores, 40 species of rodents, and four species of lagomorphs, and that I. sculptus has been recorded from humans, domestic animals (cat, dog, goat), 13 species of carnivores, 34 species of rodents, and three species of lagomorphs. In accordance with our observations from Colorado, I. kingi commonly has been found to infest heteromyid and murid rodents (such as grasshopper mice), whereas I. sculptus most frequently has been collected from ground-dwelling sciurid rodents, especially Spermophilus ground squirrels. The potential roles of I. kingi and I. sculptus as enzootic vectors of human pathogens, particularly the agents of tularemia (Francisella tularensis), Q fever (Coxiella burnetii), and Colorado tick fever (CTF virus), are discussed.     

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.     

The intraspecies variability of <Emphasis Type="Italic">Spermophilus relictus</Emphasis> sensu lato Kaschkarov 1923 (Sciuridae,Rodentia)

The intraspecies variability of Spermophilus relictus sensu lato was studied based on 27 measurements of skulls from 67 specimens of relict ground squirrels (S. relictus) and 66 specimens of Tien Shan ground squirrels (S. ralli), as well as six specimens of the relict ground squirrel from the Gissar Ridge (Tien Shan). A colorimetric analysis of skins of relict ground squirrels (19 specimens, including three individuals from the Gissar Ridge) and Tien Shan ground squirrels (19 specimens) was made. Significant intraspecies variability was found in the relict and Issyk-Kul ground squirrels, whereas the interspecies differences were small, raising questions about the species independence of the Tien Shan ground squirrel (S. ralli).     

Quantitative Shedding of Two Genotypes of Cryptosporidium parvum in California Ground Squirrels (Spermophilus beecheyi)

Sixteen percent of California ground squirrels (Spermophilus beecheyi) were found to be shedding an average of 53,875 Cryptosporidium parvum oocysts/g of feces. Male squirrels had a higher prevalence and higher intensity of shedding than did female squirrels. The majority of C. parvum isolates matched a bovine-murine genotype, with a few isolates resembling a porcine genotype. Higher intensities of shedding by males may enhance dissemination and genotypic mixing of this protozoa given males' proclivity to disperse to nonnatal colonies.     

EVOLUTIONARY RELATIONSHIPS AMONG COLONIES OF COLUMBIAN GROUND SQUIRRELS AS SHOWN BY MITOCHONDRIAL DNA

Mitochondrial DNA (mtDNA) from 71 Columbian ground squirrels (Spermophilus columbianus) collected in 12 locations in western Canada were assayed for restriction-site variation with 10 endonucleases. Five of these endonucleases revealed variant patterns, and the composite genotypes were used to develop a linear transformation series among the mtDNA genotypes. Two of the four clones had a wide distribution, while the remaining two clones were geographically restricted. The mtDNA of Columbian ground squirrels was also compared to two other species of Sciuridae: Richardson's ground squirrels (S. richardsonii) and Arctic ground squirrels (S. parryii). Calculation of divergences from fragment length and restriction-site data indicated that Arctic ground squirrels and Richardson's ground squirrels were more closely related to each other than either was to Columbian ground squirrels. The transformation series among clones within the Columbian ground squirrels was rooted using Richardson's and Arctic ground squirrels as out-groups. From these data, we conclude that the colonization by female founders of Columbian ground squirrel populations occurred after deglaciation along the eastern ranges of the Rocky Mountains, while colonies on the western ranges may have been present before extensive deglaciation occurred, having existed in refugia in northwestern Alberta.     

Spectral sensitivity of ground squirrel cones measured with ERG flicker photometry

Summary Ground squirrels have dichromatic color vision. The spectral sensitivities of the two classes of cones found in the retinas of two species of ground squirrel were measured using ERG flicker photometry. The spectral sensitivity curves for these cone classes were closely fit by curves from wavelength-dependent visual pigment nomograms. One cone type had an average peak sensitivity of 518.9 nm (California ground squirrels,Spermophilus beecheyi) or 517.0 nm (thirteen-lined ground squirrels,Spermophilus tridecemlineatus). The second type of cone found in these ground squirrels had an average peak sensitivity of 436.7 nm. An examination of the variation in spectral sensitivity among individual animals suggests that the sensitivity peaks for the middle-wavelength cone cover a range of not greater than 4 nm.     

Eimeria species (Apicomplexa: Eimeriidae) from arctic ground squirrels (Spermophilus parryii) and red squirrels (Tamiasciurus hudsonicus) in Alaska and in Siberia, Russia

Fecal samples from arctic ground squirrels (Spermophilus parryii) collected in Alaska (n = 90) and Russia (n = 46) and from red squirrels (Tamiasciurus hudsonicus) in Alaska (n = 35) were examined for the presence of Eimeria spp. (Apicomplexa: Eimeriidae). Four species were recovered from arctic ground squirrels, including Eimeria callospermophili (prevalence = 18%), Eimeria cynomysis (23.5%), Eimeria lateralis (19%), and Eimeria morainensis (77%). A single species, Eimeria tamiasciuri (91%), was recovered from red squirrels. Eimerians recovered from arctic ground squirrels represent new host records, and the single species from red squirrels is a new geographic record. Alaskan arctic ground squirrel prevalence was higher for E. callospermophili (Alaska = 22% vs. Russia = 9%), E. cynomysis (34% vs. 2%), and E. lateralis (27% vs. 4%), but not E. morainensis (78% vs. 76%).     

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.     

Effects of eimerian (Apicomplexa: Eimeriidae) infections on nutrient assimilation in the Wyoming ground squirrel.

Effects of infection with mixed species of Eimeria (E. callospermophili, E. morainensis, and E. beecheyi) on the digestive physiology of Wyoming ground squirrels (Spermophilus elegans) are described. Infected and uninfected squirrels were administered arginine and methionine in saturated glucose solution. Blood was drawn at time 0 and 30 min postadministration. Significant differences were not found between infected and uninfected squirrels in plasma glucose, arginine, or methionine assimilation. In a second experiment, infected and uninfected squirrels were fed a food slurry of known caloric value. All feces were collected for 24 hr postfeeding. Differences were not detected in fecal caloric content or digestive efficiency. These results in conjunction with results reported in the literature suggest a reassessment of the "parasitic" nature of these squirrel symbionts. We propose that associations of some Eimeria species and hosts that evolve under natural conditions are examples of parasite-host interactions that often evolve toward commensalism.     

Kin-recognition abilities and nepotism as a function of sociality

Despite widespread interest in kin selection and nepotism, relatively little is known about the perceptual abilities of animals to recognize their relatives. Here I show that a highly nepotistic species, Belding's ground squirrels (Spermophilus beldingi), produces odours from at least two sources that correlate with relatedness ('kin labels'), and that ground squirrels can use these odours to make accurate discriminations among never before encountered ('unfamiliar') kin. Recognition odours appear to vary linearly with relatedness, rather than in an all-or-none fashion, allowing precise estimates of kinship even among distant relatives. Thus S. beldingi are able to recognize their distant kin and male kin, even though they do not treat them preferentially. I also show that a closely related species (S. lateralis) similarly produces kin labels and discriminates among kin, although it shows no evidence of kin-directed behaviour. Thus, contrary to a commonly held assumption, kin favouritism and recognition abilities can evolve independently, depending on variation in the costs and benefits of nepotism for a given species.     

Absence of evidence for a hibernation "trigger" in blood dialyzate of Richardson's ground squirrel.

In order to examine evidence for a blood-borne “trigger” for mammalian hibernation, serum dialyzate from hibernating Richardson's ground squirrels (Spermophilus richardsonii) was injected into summer-active ground squirrels of the same species. Four independent trials involving 52 animals were performed. In all trials, no effect of the dialyzate was seen on nest building, weight gain or loss, or on occurrence of hibernation.     

Coccidian assemblages in the Wyoming ground squirrel, Spermophilus elegans elegans.

One thousand nineteen Wyoming ground squirrels (Spermophilus elegans elegans) from 4 populations in southern Wyoming were examined for intestinal parasites. The most prevalent parasites were 6 species of coccidia: Eimeria beecheyi, Eimeria bilamellata, Eimeria callospermophili, Eimeria larimerensis, Eimeria morainensis, and Eimeria spermophili. Most ground squirrels harbored 2 or more species. This eimerian assemblage was present across populations and over years. Differences in the prevalence of infection were not found among host age classes or between sexes. The presence or absence of helminths was independent of the presence and absence of Eimeria. A log-linear model to test the independence of the distribution of Eimeria spp. among hosts revealed 3 significant positive associations, for E. bilamellata and E. beecheyi, E. morainesis and E. callospermophili, and E. larimerensis and E. bilamellata.     

Rodent-flea-plague relationships at the higher elevations of San Diego County, California.

Rodent-flea-plague relationships were examined at sites located at higher elevations of San Diego County during 1991-2002. The most frequently sampled rodents were the California ground squirrel, Spermophilus beecheyi, and white-footed mice, Peromyscus spp. Higher seasonal mean dependent variables (prevalences of squirrels and indices of O. montana), higher mean amounts of seasonal rainfall, and lower seasonal mean ambient temperatures were found at sites during 1991--1993 compared with 2000--2002. Levels of plague antibody indicate that squirrels seroconverted at most sites during spring/early summer when exposed to infected fleas when cleaning out burrows following hibernation, when interacting more with other squirrels occurred establishing home ranges, and when dispersing juveniles occupied abandoned burrows containing old nests. The majority of squirrels (35/41) were reported seropositive at Heise County Park (elev. 1,281 m) during 1996, 2001, and 2002. This may reflect fewer fleas biting squirrels more often when squirrels spent more time below-ground in order to avoid higher ambient temperatures. In contrast, most squirrels (12/13) were reported seropositive at two higher sites (elev. 1,584 and 1,641 m) on Palomar Mountain during 1993--1996 when there were higher mean dependent variables and amounts of seasonal rainfall compared with 1999--2002. This increased rainfall may have benefited host and flea populations and thus plague transmission. Seasonal indices were usually reduced after dusting squirrel burrows with 2% diazinon dust. Findings also indicated that S. beecheyi is a primary reservoir for plague at the higher elevations of these and other sites in southern California, and that the deer mouse, Peromyscus maniculatus, and other Peromyscus spp. were not major host reservoirs at the sites sampled.     

Genetic evidence of extensive introgression of short-tailed ground squirrel genes in a hybridization zone of Spermophilus major and S. erythrogenys, inferred from sequencing of the mtDNA cytochrome b gene

We have completely sequenced the mtDNA cytochrome b gene of ground squirrels from the zone of overlapping ranges of Spermophilus major and S. erythrogenys in the Tobol-Ishim interfluve, which is a putative hybridization zone of these species. The results of the sequencing showed extensive introgression of mtDNA genes of the short-tailed ground squirrel S. e. brevicauda, whose haplotype had fully replaced the S. major haplotype. All of the ground squirrels from the Tobol-Ishim interfluve had a variant of the S. e. brevicauda mtDNA haplotype that was specific for this zone. On average, 119 substitutions (10.44%) were found between S. major from Ul'yanovsk oblast and S. e. brevicauda from the northern Kazakhstan, the mean genetic distance (D) between them being 0.115, which conforms to the corresponding parameters for the S. e. brevicauda-S. pygmaeus pair (122 substitutions, D = 0.118). Insignificant differences (seven substitutions, D = 0.043) were found between the S. major and S. pygmaeus haplotypes, which suggest that these species have similar mitochondrial haplotypes. Five to ten nucleotide substitutions (0.44–0.88%) were detected between the animals from the Tobol-Ishim interfluve and S. e. brevicauda. The mtDNA haplotype divergence D within the genus Spermophilus (ten species) for all codon positions ranged from 0.035 to 0.158. Phylogenetic reconstructions (MP, ML, and NJ trees) showed two well-differentiated clusters with high bootstrap support. However, there was different branching topology within the cluster and their species composition varied. The maximum likelihood tree, ML, differentiating the species into two subgenera, Citellus and Colobotis, most reliably reflected taxonomic relationships of the species from the genus Spermophilus, inferred from morphological and genetic biochemical data. The morphologically pure S. major (subgenus Colobotis) animals, used in the analysis, proved to carry the haplotype of another species, S. pygmaeus (subgenus Citellus). This poses a question on the existence of the specific haplotype of S. major, the reason of its replacement by haplotype of other species, and possible consequences of this phenomenon for survival of the species.     

Trypanosomes and Haemobartonella in Wild Rodents in Illinois

SYNOPSIS. Trypanosoma microti and Haemobartonella microti were found in 1 (17%) of 6 yellow-bellied voles Microtus ochrogastev , and T. iowensis was found in 7 (11.5%) of 60 thirteen-lined ground squirrels Spermophilus tridecemlineatus in Illinois. Reports of lewisi group trypanosomes from Microtus and Spermophilus are summarized. Those from different rodent host genera are considered to belong to different species. All of the 6 species named from the host genus Sperinophilus may belong to a single species; if so, their correct name would be T. otospermophili. However, until adequate cross transmission studies are carried out, it is considered preferable to retain the names originally assigned to the North American species.