| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1 Department of Veterinary Pathology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B4, Canada
2 Department of Large Animal Clinical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B4, Canada
3 Canadian Co-operative Wildlife Health Centre, Department of Veterinary Pathology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B4, Canada
5 Corresponding author (email: cjardi01{at}uoguelph.ca)
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
2 yr old were infected with Bartonella. Prevalence of infection was lowest in May (27%) and highest in late summer and early autumn (71%). The prevalence of fleas also varied seasonally, and animals were more likely to have fleas in the late summer and early autumn than in early summer. We found no relationship between Bartonella prevalence and host density or flea prevalence. |
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Evidence that rodent-associated Bartonella can cause human disease has led to numerous cross-sectional surveys, which have found high prevalence of Bartonella in a variety of rodents at many locations (Birtles et al., 1994; Kosoy et al., 1997). Although useful for identifying potential rodent reservoirs of Bartonella, cross-sectional studies do not explain how these bacteria are maintained and transmitted among their rodent hosts.
Longitudinal and multiple cross-sectional studies at the same sites allow us to determine the dynamics of infectious agents in their reservoir hosts, which may aid in understanding when and why these agents "emerge" to infect humans. There have been three longitudinal studies of Bartonella in wild rodents that have provided valuable information about the dynamics of Bartonella infections. Kosoy et al. (2004) described the demographic and temporal patterns of Bartonella infections in cotton rats (Sigmodon hispidus) in the USA. Fichet-Calvet et al. (2000) studied Bartonella in fat sand rats (Psammomys obesus) in Tunisia, and Birtles et al. (2001) studied the dynamics of Bartonella infections in 12 rodent hosts in the UK. Such studies, in a variety of rodent hosts, at a variety of locations, are needed to determine if any general conclusions can be made about the dynamics of Bartonella infections in wild rodents.
In a previous study, we found that 49% of Richardson’s ground squirrels (Spermophilus richardsonii), which are semi-colonial rodents that are common on the Canadian prairie, were infected with Bartonella sp. (Jardine et al., 2005). Here we present temporal, age, and sex-specific demographics of Bartonella infections in Richardson’s ground squirrels.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
We conducted this study as a repeated cross-sectional study of 11 Richardson’s ground squirrel populations. We did recapture some individuals and accounted for repeat captures of individual squirrels in our analysis.
Trapping and processing
Procedures for trapping and handling rodents were approved by the animal care committee at the University of Saskatchewan (University Committee on Animal Care and Supply Protocol 2020028). Richardson’s ground squirrels were trapped live at up to 11 sites around Saskatoon, Saskatchewan, from April to September in 2002, 2003, and 2004, using unbaited burrow traps (Wobeser and Leighton, 1979) placed in burrow entrances where squirrels were seen. Sites were chosen based on known presence of Richardson’s ground squirrels and their proximity to the laboratory. Sites used in the study varied from year to year because of changes in land use and study design (Table 1
). In 2002, sites were trapped for only a portion of 1 day for 1 or 2 mo in the summer. In 2003 and 2004, sites were trapped from approximately 1 hr after sunrise until 1 hr after midday, for 2 to 3 days each month, starting in April or May.
|
Numbered metal ear tags (#1005-1; National Band and Tag Co., Kentucky, USA) were placed in both ears for subsequent identification, and sex, age (adult or juvenile), and mass were recorded for each animal. Blood was collected by cardiac puncture from animals that were to be euthanized and from the medial saphenous vein of animals that were to be released. In 2003 and 2004, we examined and brushed each animal for 3 min and recorded the presence or absence of fleas and ticks.
All euthanized animals were necropsied, and tissues were held frozen at –70 C or in 10% neutral buffered formalin as appropriate for subsequent examination. Blood samples were placed in liquid nitrogen in the field and then transferred to a –70 C freezer for storage.
Population density estimates
We did not estimate squirrel density in 2002. Direct counts are considered to be reliable for estimating squirrel population density because squirrels are "easily spotted, rather sedentary, and colonial, and their activity correlates well with weather conditions" (Zegers, 1982). We estimated squirrel population density twice per year in 2003 and 2004 based on: 1) the number of animals trapped in early May when all adults were aboveground and juveniles had not yet emerged from their natal burrows; and 2) on the number of animals trapped in June when all juveniles had emerged from their natal burrows and adults were still aboveground. Ten squirrels that were caught prior to and after, but not during, the census period were included in the estimates. For the sites where the trapped area was a portion of a larger colony, we estimated the effective trapping area by adding an area equal to half the mean of the maximum distance moved by squirrels caught in multiple sessions (Wilson and Anderson, 1985). For sites where traps were set over the entire colony, we used the area of the colony with no buffer.
Bartonella isolation
Published procedures for isolating Bartonella from blood (Kosoy et al., 1997) were used. Briefly, 0.15 ml of whole blood was plated on commercial sheep blood agar (BBC Columbia Agar; Becton Dickinson Company, Sparks, Maryland, USA) and on ATCC GC Agar medium prepared at our institution, and plates were incubated at 37 C in an aerobic atmosphere with 7% carbon dioxide for up to 30 days. The plates were checked twice weekly for growth, and isolated colonies were subcultured to confirm purity. Bacterial colonies were tentatively identified as Bartonella based on morphology and standard biochemical tests (Welch and Slater, 1999). All morphologically distinct colony types from each sample were identified individually. The level of bacteremia was classified as low if there were fewer than ten colony-forming units (CFU) and high if there were ten or more CFU on the original plate. This cutoff point was selected as a midpoint in a bimodal distribution of the data.
Bartonella polymerase chain reaction
DNA was extracted using a standard phenol-chloroform extraction from bacterial colonies that were tentatively identified as Bartonella. The extracted DNA was stored in TE buffer at –70 C prior to polymerase chain reaction (PCR) amplification.
Two oligonucleotides (BhCs781.p and BhCs1137.n), specific for the citrate synthase (gltA) gene of Bartonella, were used as PCR primers, resulting in a 379 base pair product (Norman et al., 1995). The PCR mixture consisted of 2 µl of sample DNA, 35.25 µl of sterile ultrapure water, 5 µl of 10X PCR buffer, 3 µl of (25 mM) MgCl2, 0.5 µl (25 mM) dNTPs, 2 µl (20 pmol) of each primer, and 0.25 µl (5 U/µl) Taq polymerase, resulting in a total volume of 50 µl. PCR amplifications were carried out in a PTC200 DNA-Engine (MJ Research, Watertown, Massachusetts, USA). The mixture was incubated at 94 C for 2 min, then amplified for 40 cycles at 94 C for 30 sec, 50 C for 60 sec, and 72 C for 60 sec, then held at 72 C for 5 min. To visualize the PCR amplicons, PCR products were separated by electrophoresis in 1.25% agarose gel with ethidium bromide staining, according to standard methods.
Data analysis
We examined the associations between various demographic factors and Bartonella prevalence, flea prevalence, and prevalence of a high level of bacteremia using multilevel mixed models, which allowed us to account for clustering of individual animals within a site using random intercepts for the site and to account for repeated measures within individual animals over time (MLwiN version 2.0, Centre for Multilevel Modelling, London, UK). A binomial distribution and logit link function were used to model all outcomes. Factors examined for association with Bartonella prevalence included year, month, age, sex, population density, and flea prevalence. Factors examined for association with flea prevalence and prevalence of high level bacteremia were year, month, age, and sex. For each outcome, all factors with P < 0.25 on their own (univariate models) were combined and backward elimination was used to identify a final (multivariate) model. All factors where P < 0.05 were considered statistically significant.
Monthly prevalence estimates and 95% confidence intervals for Bartonella, fleas, and high level of bacteremia were calculated using MLwiN models, taking into account clustering of individual animals within site and year (Dohoo et al., 2003).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
The proportion of adults and juveniles making up the trapped population varied throughout the summer (Fig. 1). Primarily adult animals were trapped in April and May, and juveniles only began to enter traps after emerging from their natal burrows at the end of May. The proportion of trapped animals that were adult declined over the summer, with adults representing only 4% of animals trapped in August and September. The sex ratio of adult ground squirrels in April was four females/male, which is typical for adults of this species (Michener and Michener, 1977). Juveniles did not show the same skewed sex ratio: 102 of 222 (46%) juveniles trapped in June were males. The proportion of juvenile males in the trapped population increased over the summer to 67% (18 of 27 animals) by September.
|
Of 781 blood samples collected from Richardson’s ground squirrels captured at ten sites in 2002, 2003, and 2004, 585 (75%) were submitted for Bartonella culture. The overall prevalence of Bartonella infection, based on culture and confirmed by PCR, was 48%. This estimate of prevalence includes multiple samples from individual squirrels captured in more than one monthly trapping session. Our estimate of prevalence remains the same (48% of 368) if we include only results from first capture samples; however, our estimate of Bartonella prevalence increases to 57% if we count an animal as positive if it was positive at any of the times it was sampled. The likelihood of detecting Bartonella infections in individual animals increased with the number of times it was sampled. Of 92 animals sampled twice, 68% were Bartonella positive at least once and 74% of 46 animals sampled on three or more occasions were positive for Bartonella at least once.
The estimated density of ground squirrels on areas trapped in 2003 and 2004 ranged from five to 38 animals/ha (average 18/ha) in May and from 14 to 60 animals/ ha in June (average 40/ha) (Table 2). Squirrel density was not associated with Bartonella prevalence (P = 0.72, Fig. 2).
|
|
).
|
). In our final model, after adjusting for age and year, infection with Bartonella was significantly more likely in April, July, August, and September compared with June (Table 3
).
|
). In a small subset of animals of known age, we found that 58% of 24 animals known to be 1 year of age were infected with Bartonella, whereas, only 24% of 25 animals known to be 2 years of age animals were infected with Bartonella. More males (58%) than females (43%) were positive for Bartonella (203 and 382 animals tested, respectively). Although males were significantly more likely to have Bartonella infections in our univariate model (P = 0.001), after adjusting for age, year, and month, we found that there was no significant difference in the prevalence of Bartonella infections between males and females (P = 0.14). Therefore, sex was not included as a factor in our final model.
Flea prevalence was included as a factor in building our final model (P = 0.1 in univariate model); however, because month and flea prevalence varied collinearly, we could not include them both in the same model. No relationship was found between the prevalence of Bartonella infections and flea prevalence after adjusting for age and year (P = 0.22, Fig. 4), so flea prevalence was excluded in our final model. Month, as discussed previously, remained significant after adjusting for age and year, and was included in our final model (Table 3).
|
Fleas were found on 82% of 465 animals examined. Ticks were detected on only 8% of 455 animals examined. Due to the small number of ticks detected, we considered only fleas for further analysis.
Fleas were found on 81% of female and 84% of male animals examined (286 and 179 animals examined, respectively). There was no significant difference in flea prevalence on male and female ground squirrels (P = 0.29).
Fleas were found on 82% of 208 animals examined in 2003 and 83% of 257 animals examined in 2004, and there was no significant difference in prevalence of fleas between years after adjusting for age and month (P = 0.53); therefore, year was not included in our final model. The prevalence of fleas on ground squirrels varied seasonally, decreasing from 87% in April to 74% in June and then increasing to 99% by August–September (Fig. 5). We combined August and September for the analysis due to the small sample size in September. The prevalence of fleas on Richardson’s ground squirrels was significantly higher in July and August–September than in June in our final model (after adjusting for age) (Table 4).
|
|
). Bartonella bacteremia
The level of bacteremia (high or low) was determined for 233 animals infected with Bartonella. Overall, 46% of animals had a low level of bacteremia and 54% had high levels of bacteremia.
In 2003, the majority of animals, from which Bartonella was isolated, had high levels of bacteremia (57% of 167 animals tested), while 47% of animals in 2004 had high levels of bacteremia (66 animals tested). The difference between years was not significant after adjusting for age and month (P = 0.1) and was not included in our final model. The proportion of Bartonella-positive animals with a high level of bacteremia varied throughout the summer, increasing from 40% in April to 69% in July and then decreasing to 47% in September (Fig. 6), but there was no difference in the monthly proportions of animals with high levels of bacteremia after adjusting for age and year (P = 0.36). Therefore month was not included in the final model.
|
Males and females infected with Bartonella were equally likely to have high levels of bacteremia (54% of 136 females and 54% of 97 males; P = 0.9).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
We found no relationship between host density and Bartonella prevalence in this study. In contrast, Fichet-Calvet et al. (2000) found an inverse relationship between prevalence of infection with Bartonella and host abundance. Ideally, to investigate whether Bartonella prevalence is related to host density, the prevalence of Bartonella should be determined for multiple independent sites with different host densities. We attempted to do this, but our sample size was very small, and our estimates were not all independent (we used the same sites within and among years). Therefore, we cannot rule out that there was a relationship that we were unable to detect. An alternative approach for investigating the relationship between host abundance and Bartonella prevalence would be to experimentally reduce or increase host density.
The temporal patterns seen in this study are similar to those reported in other longitudinal studies of Bartonella (Fichet-Calvet et al., 2000; Kosoy et al., 2004), with high levels of infection occurring in late summer and autumn. A significant proportion of adult squirrels (51%) were infected with Bartonella during the first trapping session in April. Because Richardson’s ground squirrels hibernate over winter, this suggests that infections are maintained either in the squirrels or ectoparasites over the winter. We found that the prevalence of Bartonella decreased in the early summer as reported by Kosoy et al. (2004). In our study, the prevalence was lowest in May, which corresponds to the first few weeks of life for juvenile squirrels before they emerge from their natal burrows. Once juveniles emerge in late May, the prevalence of Bartonella increased for the remainder of the summer, with the majority of juvenile animals developing Bartonella bacteremia after emerging from their natal burrows. Not only was the prevalence of Bartonella infections highest in the late summer, but the prevalence of fleas was also greatest at this time, making the late summer the period of greatest risk for transmission of the bacteria among squirrels and potentially to other species, including humans.
Juvenile animals were significantly more likely to be infected with Bartonella than were adult animals (58% and 37%, respectively), and were more likely to have high levels of bacteremia. Although we did not know the exact age of all adult ground squirrels, only 24% of animals that were known to be 2 years old were infected with Bartonella. Kosoy et al. (2004) also reported that the prevalence of Bartonella infections decreased with age and Kosoy et al. (2004) and Fichet-Calvet et al. (2000) found that juvenile animals had significantly higher bacterial loads than adult animals.
Decreasing prevalence with age combined with lower levels of bacteremia in older animals suggest that animals are able to clear infections through acquired immunity (Kosoy et al., 2004). In experimental infections, antibodies play an essential role in terminating B. grahamii infections in laboratory mice (Koesling et al., 2001). We did not measure antibodies in this study. Kosoy et al. (2004) found few animals with antibodies (15%) in a longitudinal field study, and the majority of animals with antibodies had very low titers, suggesting that antibody production is not a feature of Bartonella infections in, at least some, species of wild rodents in North America.
Alternatively, a low prevalence of Bartonella in older animals might indicate that animals infected with Bartonella are less likely to survive. Boulouis et al. (2001) found no difference in survival of experimentally infected and noninfected rodents, and Fichet-Calvet et al. (2000) reported no differences in the weight of Bartonella infected and noninfected animals in the field. However, there may be species differences in effects on rodent hosts, and it also is possible that the effects of the bacteria are subtle; for example, Bartonella may cause chronic disease, which may affect survival only later in life. Because the majority of Richardson’s ground squirrels are infected at some point in their life (74% sampled three or more times in this study were positive for Bartonella at least once), it is difficult to compare survival rates of infected and noninfected animals. Determination of the "cost" of Bartonella infections to their hosts remains an area for future research.
Ectoparasites have been implicated as potential vectors for Bartonella in rodents (Bown et al., 2003; Durden et al., 2004). Ticks were found on only 8% of Richardson’s ground squirrels in this study, and Hilton and Mahrt (1971) found that only 2% of Richardson’s ground squirrels sampled in Alberta, Canada, were infested with ticks. Because ticks occur uncommonly on Richardson’s ground squirrels, it is unlikely that they would be important vectors of Bartonella for this species. We found fleas on more than 80% of animals examined. Although we did not find a significant relationship between the occurrence of fleas on animals and Bartonella prevalence in this study, it is interesting that, based on monthly prevalence levels, these two factors appear to vary in parallel (Figs. 3, 5). High flea prevalence in all months combined with relatively small sample sizes make it difficult to detect any relationship that might be present.
We found that infections with Bartonella were less common in ground squirrels in 2004 than in 2003 or 2002. Although it is beyond the scope of this study to determine why fewer ground squirrels were infected with Bartonella in 2004, it should be noted that the summer of 2004 was the coolest and wettest of the three years included in this study. It would be interesting to determine if our findings are consistent and if they are related to how ectoparasites fare in different climatic conditions. Although we found no difference in the prevalence of fleas on squirrels in 2003 and 2004, we did not measure the intensity of flea infestations. Ryckman (1971) found that, during the summer months, the number of fleas on California ground squirrels was lower in experimental areas where natural precipitation was supplemented with water sprinklers. It is possible that the number of fleas per host, not just the presence of fleas on a host, is an important factor influencing the transmission of the bacteria. Separating the relationships among climatic conditions, ectoparasites, and Bartonella prevalence will require long-term studies.
We did not sequence the isolates that were found in this study, and some of the demographic and temporal features that we report may be a consequence of Richardson’s ground squirrels acquiring and losing infections with different genotypes of Bartonella. The purpose of this paper was to present the demographic and temporal features of Bartonella infections in Richardson’s ground squirrels in a general sense. Future research will be required to determine the mechanism for the findings in this study.
Description and understanding of the ecology of zoonotic pathogens in their reservoir hosts are essential for predicting and preventing disease occurrence in humans. We are only beginning to unravel the complex relationships between Bartonella spp. hosts and vectors.
|
ACKNOWLEDGMENTS |
|---|
|
FOOTNOTES |
|---|
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
———, N. A. SAUNDERS, AND ———. 1995. Proposals to unify the genera Grahamella and Bartonella, with descriptions of Bartonella talpae comb. nov., Bartonella peromysci comb. nov., and three new species, Bartonella grahamii sp. nov., Bartonella taylorii sp. nov., and Bartonella doshiae sp. nov. International Journal of Systematic Bacteriology 45: 1–8.
———, S. M. HAZEL, M. BENNETT, K. BOWN, D. RAOULT, AND M. BEGON. 2001. Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiology and Infection 126: 323–329.[Medline]
BOULOUIS, H. J., F. BARRAT, D. BERMOND, F. BERNEX, D. THIBAULT, R. HELLER, J. J. FONTAINE, Y. PIEMONT, AND B. B. CHOMEL. 2001. Kinetics of Bartonella birtlesii infection in experimentally infected mice and pathogenic effect on reproductive functions. Infection and Immunity 69: 5313–5317.
BOWN, K. J., M. BENNETT, AND M. BEGON. 2004. Flea-borne Bartonella grahamii and Bartonella taylorii in bank voles. Emerging Infectious Diseases 10: 684–687.[Medline]
CHOMEL, B. B., A. C. WEY, AND R. W. KASTEN. 2003. Isolation of Bartonella washoensis from a dog with mitral valve endocarditis. Journal of Clinical Microbiology 41: 5327–5332.
DALY, J. S., M. G. WORTHINGTON, D. J. BRENNER, C. W. MOSS, D. G. HOLLIS, R. S. WEYANT, A. G. STEIGERWALT, R. E. WEAVER, M. I. DANESHVAR, AND S. P. O’CONNER. 1993. Rochalimaea-Elizabethae sp-nov isolated from a patient with endocarditis. Journal of Clinical Microbiology 31: 872–881.
DEHIO, C. 2004. Molecular and cellular basis of Bartonella pathogenesis. Annual Review of Microbiology 58: 365–390.[Medline]
DOHOO, I., W. MARTIN, AND H. STRYHN. 2003. Veterinary Epidemiologic Research, AVC Inc. Charlottetown, PEI, 706 pp.
DURDEN, L. A., B. A. ELLIS, C. W. BANKS, J. D. CROWE, AND J. H. OLIVER. 2004. Ectoparasites of gray squirrels in two different habitats and screening of selected ectoparasites for bartonellae. Journal of Parasitology 90: 485–489.[Medline]
ELLIS, B. A., R. L. REGNERY, L. BEATI, F. BACELLAR, M. ROOD, G. G. GLASS, E. MARSTON, T. G. KSIAZEK, D. JONES, AND J. E. CHILDS. 1999. Rats of the genus Rattus are reservoir hosts for pathogenic Bartonella species: An Old World origin for a New World disease? Journal of Infectious Disease 180: 220–224.[Medline]
FICHET-CALVET, E., I. JOMAA, R. BEN ISMAIL, AND R. W. ASHFORD. 2000. Patterns of infection of haemoparasites in the fat sand rat, Psammomys obesus, in Tunisia, and effect on the host. Annals of Tropical Medicine and Parasitology 94: 55–68.[Medline]
HILTON, D. F., AND J. L. MAHRT. 1971. Ectoparasites from three species of Spermophilus (Rodentia: Sciuridae) in Alberta. Canadian Journal of Zoology 49: 1501–1504.[Medline]
HOLMBERG, M., J. N. MILLS, S. MCGILL, G. BENJAMIN, AND B. A. ELLIS. 2003. Bartonella infection in sylvatic small mammals of central Sweden. Epidemiology and Infection 130: 149–157.[Medline]
JARDINE, C., G. APPLEYARD, M. Y. KOSOY, D. MCCOLL, M. CHIRINO-TREJO, G. WOBESER, AND F. A. LEIGHTON. 2005. Rodent-associated Bartonella in Saskatchewan, Canada. Vector-Borne and Zoonotic Diseases 5: 402–409.
KERKHOFF, F. T., A. M. C. BERGMANS, A. VAN dER ZEE, AND A. ROTHOVA. 1999. Demonstration of Bartonella grahamii DNA in ocular fluids of a patient with neuroretinitis. Journal of Clinical Microbiology 37: 4034–4038.
KOESLING, J., T. AEBISCHER, C. FALCH, R. SCHULEIN, AND C. DEHIO. 2001. Cutting edge: Antibody-mediated cessation of hemotropic infection by the intraerythrocytic mouse pathogen Bartonella grahamii. Journal of Immunology 167: 11–14.
KOSOY, M., R. L. REGNERY, T. TZIANABOS, E. L. MARSTON, D. C. JONES, D. GREEN, G. O. MAUPIN, J. G. OLSON, AND J. E. CHILDS. 1997. Distribution, diversity, and host specificity of Bartonella in rodents from the southeastern United States. American Journal of Tropical Medicine and Hygiene 57: 578–588.
———, M. MURRAY, R. D. GILMORE, Y. BAI, AND K. L. GAGE. 2003. Bartonella strains from ground squirrels are identical to Bartonella washoensis isolated from a human patient. Journal of Clinical Microbiology 41: 645–650.
———, E. MANDEL, D. GREEN, E. MARSTON, AND J. CHILDS. 2004. Prospective studies of Bartonella of rodents. Part I. Demographic and temporal patterns in population dynamics. Vector-Borne and Zoonotic Diseases 4: 285–295.
MEXAS, A. M., S. I. HANCOCK, AND E. B. BREITSCH-WERDT. 2002. Bartonella henselae and Bartonella elizabethae as potential canine pathogens. Journal of Clinical Microbiology 40: 4670–4674.
MICHENER, G. R., AND D. R. MICHENER. 1977. Population structure and dispersal in Richardson’s ground squirrels. Ecology 58: 359–368.
MILLS, J. N., T. L. YATES, J. E. CHILDS, R. R. PARMENTER, T. G. KSIAZEK, P. E. ROLLIN, AND C. J. PETERS. 1995. Guidelines for working with rodents potentially infected with hantavirus. Journal of Mammalogy 76: 716–722.
NORMAN, A. F., R. REGNERY, P. JAMESON, C. GREENE, AND D. C. KRAUSE. 1995. Differentiation of Bartonella-like isolates at the species level by PCR-restriction fragment length polymorphism in the citrate synthase gene. Journal of Clinical Microbiology 33: 1797–1803.[Abstract]
RYCKMAN, R. E. 1971. Plague vector studies. Part II. The role of climactic factors in determining seasonal fluctuations of flea species associated with the California ground squirrel. Journal of Medical Entomology 8: 541–549.[Medline]
WELCH, D. F., AND L. N. SLATER. 1999. Bartonella and Afipia. In Manual of clinical microbiology, P. R. Murray, E. J. Baron, M. A. Pfaller, F. C. Tenover and R. H. Yolken (eds.). American Society for Microbiology, Washington, D.C., pp. 638–645.
———, K. C. CARROLL, E. K. HOFMEISTER, D. H. PERSING, D. A. ROBISON, A. G. STEIGERWALT, AND D. J. BRENNER. 1999. Isolation of a new subspecies, Bartonella vinsonii subsp. arupensis, from a cattle rancher: Identity with isolates found in conjunction with Borrelia burgdorferi and Babesia microti among naturally infected mice. Journal of Clinical Microbiology 37: 2598–2601.
WILSON, K. R., AND D. R. ANDERSON. 1985. Evaluation of two density estimators of small mammal population size. Journal of Mammalogy 66: 13–21.
WOBESER, G. A., AND F. A. LEIGHTON. 1979. A simple burrow entrance live trap for ground squirrels. Journal of Wildlife Management 43: 571–572.
YING, B., M. Y. KOSOY, G. O. MAUPIN, K. R. TSUCHIYA, AND K. L. GAGE. 2002. Genetic and ecologic characteristics of Bartonella communities in rodents in southern China. American Journal of Tropical Medicine and Hygiene 66: 622–627.[Abstract]
ZEGERS, D. A. 1982. Richardson’s ground squirrel. In CRC handbook of census methods for terrestrial vertebrates, D. E. Davis (ed.). CRC Press Inc., Boca Raton, Florida, pp. 152–153.
Received for publication 4 November 2005.
This article has been cited by other articles:
|
|
 |
|
  C. Jardine, C. Waldner, G. Wobeser, and F. A. Leighton EFFECT OF EXPERIMENTAL ECTOPARASITE CONTROL ON BARTONELLA INFECTIONS IN WILD RICHARDSON'S GROUND SQUIRRELS J. Wildl. Dis., October 1, 2006; 42(4): 750 - 758. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
