Determination of hantavirus distribution in northeast Missouri small mammal communities.

Abstract:

Hantavirus pulmonary syndrome (HPS) is a frequently fatal rodent-borne zoonosis that is endemic in the Americas. Although human cases of HPS have yet to be reported in Missouri, previous studies have established that white-footed mice and prairie voles are naturally associated with hantaviruses in northeastern and central Missouri. The purpose of this study was to determine seroprevalence levels in local rodents and to investigate patterns of seroprevalence among habitats common to the northeast Missouri. Wild rodents were captured at 5 localities within Adair, Chariton, and Schuyler counties (northeastern Missouri) during the summer of 2003. Overall trap success was 183 rodents/3870 total trap-nights or 4.73%. Blood samples from the rodents were tested for antibody (IgG) to a hantavirus, using an enzyme-linked immunosorbent assay. Antibody to a hantavirus was found in 11 of 106 white-footed mice (Peromyscus leucopus), and none of the 31 other rodents tested, that is--19 deer mice (P. maniculatus), 2 harvest mice (Reithrodontomys megalotis), and 10 voles (Microtus ochrogaster). Eighty-one percent of the seropositive rodents occurred in oak-hickory forest, the preferred habitat of P. leucopus, with 9% in each peridomestic and disturbed grassland habitats, respectively. Subsequent extraction and sequencing of viral mRNA from a subset of these seropositive rodents resulted in documentation of Sin Nombre Hantavirus (strain Blue River). The presence of a hantavirus known to cause HPS makes an understanding of rodent hantavirus seroprevalence across species and habitat types critical for prevention of disease in human populations.

Keywords:

Hantavirus, Peromyscus leucopus, Missouri

1. Introduction

Murid rodents (family Muridae) in the subfamilies Sigmodontinae (New World mice and rats), Murinae (Old World rats and mice), and Arvicolinae (voles) are the principal hosts of the hantaviruses known to cause human disease (Schmaljohn and Hjelle, 1997). Specific rodents (usually one or two closely related species) are the principal hosts of the North American hantaviruses for which natural host relationships have been studied extensively (Table 1). Human Hantavirus pulmonary syndrome (HPS) is a frequently fatal pneumonia-like disease caused by hantaviruses principally associated with sigmodontine rodents. These viruses are usually transmitted from rodent-to-rodent and from rodent-to-human via direct contact with blood or saliva through bites or scratches, and more commonly by inhalation of aerosols created from disruption of dried urine or feces. Exposure frequently occurs indoors during activities such as sweeping closets. Flu-like symptoms typically appear 1-5 weeks post-exposure and are subsequently followed by pulmonary edema resulting in a fatality rate of 38% (Khan et. a12000). Hantavirus pulmonary syndrome is a documented threat to farm and domestic workers, field biologists, and fire/building inspectors (Mills et. a12002). In July 2004, a mammalogy graduate student died of HPS following a small mammal survey in West Virginia (MMWR 2004).

Seven rodent species indigenous to Missouri are naturally associated with hantaviruses. These include the deer mouse (Peromyscus maniculatus), white-footed mouse (P. leucopus), prairie vole (Microtus ochrogaster), meadow vole (M. pennsylvanicus), harvest mouse (Reithrodontomys megalotis), cotton rat (Sigmodon hispidus), and marsh rice rat (Oryzomys palustrus). Previous studies have revealed antibodies to Sin Nombre Hantavirus (strain Blue River-Missouri) in white-footed mice (P. leucopus) captured in Adair County, Missouri (Monroe 1999). Two additional instances of rodent hantavirus infection were reported in central Missouri in Pulaski and St. Louis Counties within the prairie vole Microtus ochrogaster (Scharninghausen et. al 1994). However, no extensive baseline presence or absence data exists for Hantavirus in northeast Missouri, although P. maniculatus, P. leucopus, M. pennsylvanicus, and M. ochrogaster, and R. megalotis are commonly and consistently captured in the region.

Knowledge of the geographical distribution of the hantaviruses that cause human disease is essential to understand the risk of infection in humans. This is especially important as HPS has yet to be reported in Missouri, yet the majority of neighboring states have reported 2 or more cases (CDC 2005). Thus, the objectives of this study were to establish baseline Hantavirus seroprevalence in northeast Missouri rodents and investigate associations between ecological factors and rodent seroprevalence.

2. Material and Methods

To determine baseline presence/absence data for hantavirus in northeast Missouri, five localities were selected for sampling within Adair, Chariton, and Schuyler counties. Each locality was sampled according to habitat type, with habitat type based on anthropogenic usage of particular areas, i.e. peridomestic, hay fields, corn fields, disturbed grasslands, oak-hickory forest, and restored prairie. This classification scheme attempts to distinguish areas based upon human use patterns and potential rodent contact. Peridomestic sites were located at the Truman State University Farm in Adair County (N 40[degrees] 10' 48.6" W 92[degrees] 36' 2.1" 361m), and private land in Schuyler Co (N 40[degrees] 18' 40.44" W 92[degrees] 36' 1.08"). Forest sites were located at Sugar Creek Conservation Area in Adair County (N 40[degrees] 12' 1.38" W 92[degrees] 64' 2.1") and Swan Lake National Wildlife Refuge in Chariton County (N 39[degrees] 34' 30.96" W 93[degrees] 12' 20.88"). Disturbed grassland sites were located in Big Creek Conservation area in Adair County (N 40[degrees] 17' 2.1" W 92[degrees] 61' 46.74" 276m). The native grassland site was located on private land in Schuyler county and was restored by a botanist affiliated with Truman State University (N 40[degrees] 18' 37.2" W 92[degrees] 35'47.52"). The agriculture sites were represented by both corn and hay fields. The cornfield was located in Chariton County at Swan Lake Wildlife Refuge (N 39[degrees] 36' 33.96" W 93[degrees] 13' 31.56"). The hay fields were located in Adair County at the Truman State University Farm (N 40[degrees] 10' 48.6" W 92[degrees] 36' 2.1" 361m) and private land in Schuyler county (N 40[degrees] 18' 37.86" W 92[degrees] 36' 4.08" 283m). Latitude and longitude were determined by a handheld GPS unit and photographs were taken to document the habitat (Mills 2002).

Each site was sampled for four consecutive nights using approximately 125 live folding Sherman traps (H.B. Sherman Traps, Tallahassee FL) set equally spaced in transects (approximately 500 trap nights per site). Traps were baited with peanut butter and oatmeal. Safety protocols defined by Mills (2002) of the Centers for Disease Control were followed to ensure personal safety and reduce animal stress. Double latex gloves, disposable hospital gowns, and HEPA air filtration devices were worn during animal processing. Animals were euthanized in Ziplock bags with chloroform and placed on a sterilized surface for standard measurements including species, age, sex, mass, total body length, tail length, right hind foot length, ear length, reproductive status, and presence of wounds or scars. Each specimen was assigned a unique Truman Kryovoucher number and presence of wounds and ectoparasites was recorded. Liver, kidney, heart, and lung tissue samples were obtained via a longitudinal incision of the abdominal wall and removed with sterile forceps. Tissues were stored on dry ice until placed in a -80 degree Celsius freezer. Tissues were subsequently used for attempted viral isolation and messenger ribonucleic acid sequencing at UT-Galveston. Blood samples were collected from pooled abdominal blood using Nobuto strips (Advantec; Dublin, CA). Saturated strips were allowed to air dry and were sent to UT-Galveston for ELISA analysis. Samples were analyzed according to procedures set forth in Mantooth (2001). However, after sample collection, it was determined that the serological methods employed did not allow for analysis of Microtus samples. Therefore, Microtus samples are excluded from analyses.

After initial processing, carcasses of Peromyscus and Microtus were disinfected in 95% ethanol for at least 48 hours prior to preparation as a standard museum voucher and deposited into the Truman State Natural History Collection. All materials, including traps, were cleaned using a commercial Lysol and water solution. Cleaned traps were replaced to the existing transects, and all traps were rebaited for the following night.

3. Results

A total of 3870 trap nights between May and August 2003 resulted in 137 sigmodontine rodent captures (183 total). Capture results by species are summarized in Table 2 and trapping effort is given in Table 3. Captures included Peromyscus leucopus, Peromyscus maniculatus, Microtus ochrogaster, Mus musculus and Reithrodontomys megalotis. The house mouse, Mus musculus, was not sampled because it is not rodent vector for the virus of interest. Its capture did affect total success and is mentioned in Table 1 and 2, respectively. Eleven Peromyscus leucopus were seropositive to a hantavirus by ELISA analysis of blood samples. These individuals represented approximately 10% of sampled P. leucopus and 8% of total rodent captures.

Seropositive P. leucopus were differentially dispersed across the habitat types sampled with 81% of the seropositive rodents captured in oak hickory forest habitat. Additionally, peridomestic areas and hay fields each produced 9% of the remaining seropositive animals, respectively (Fig. 1). It is important to note that each habitat type was sampled for a minimum of 500 trap nights, however, due to collaborative opportunities some habitat types have data available for more than 500 trap nights. Nonetheless, the inequality of trap nights across habitat types did not necessarily affect the distribution of seropositive rodents captured (Table 1-2). The oak-hickory forest site at Swan Lake had 9 seropositive individuals for 460 trap nights, while 635 trap nights in an Agriculture-Hay site in Schuyler county produced 1 seropositive individual.

[FIGURE 1 OMITTED]

Tissues from a subset of the seropositive individuals were subjected to viral mRNA isolation and sequencing. Sequence analysis revealed the hantavirus present to be Blue River-Missouri, which has very recently been reclassified as species Sin Nombre, strain Blue River-Missouri (Cooper et al., manuscript in prep; Nichol et al., 2005). The viral species Sin Nombre has been implicated in HPS, however, the Blue River strain has unknown pathogenicity.

4. Discussion

Sampling of rodent communities in three counties and across varied habitat types verified the presence of antibodies to a hantavirus in P. leucopus in northeast Missouri. Further work determined the viral identity to be Sin Nombre Blue River-Missouri. The seropositive rodents primarily resided in oak-hickory forest habitat, not surprising due to the semi-arboreal nature of P. leucopus. Seropositive rodents not only came from three habitat types, but the sites were located in distinct counties (Oak Hickory-Chariton Co, Peridomestic-Adair Co, and Hayfield- Schuyler Co). Specifically the forest site was located at Swan Lake National Wildlife Refuge, the peridomestic site was the perimeter of a building at the Truman State University Farm in Kirksville, and the hayfield was located on private land in Schuyler Co. (Figure 2). Therefore, the seropositive samples detected in this study were located in geographically disparate areas and suggests widespread prevalence of hantavirus in the region and the likely presence of the virus in intervening counties not yet surveyed.

[FIGURE 2 OMITTED]

The number of Missouri rodents seropositive to Hantavirus is similar to studies from nearby states. A similar study conducted in Indiana by Dietrich et al. in 1997, captured 69 sigmodontine rodents from 3 counties and found 6 Peromyscus leucopus seropositive to Sin Nombre Hantavirus (strain Blue River-Indiana). In that study, P. leucopus represented 94% of total captures (65 of 69), with other species including Microtus pennsylvanicus, Zapus hudsonius, and Blarina brevicauda. Only P. leucopus was seropositive, with approximately 9% of these animals seropositive to the Blue River-Indiana strain of Sin Nombre Hantavirus. These seropositive rodents represented approximately 8.5% of total captures. This compares closely to the 10% seropositive rate found in northeast Missouri.

Data on trapping effort and capture success verify that methods employed successfully resulted in capture of primarily sigmodontine rodents. Capture distribution by species shows differential capture of rodents by habitat type and locality, which is important to consider when looking at the distribution of seropositive animals. Missouri P. leucopus prefer oak-hickory forest, but can generalize their habitat preferences (Schwartz 2001). Thus, they were primarily captured in oak-hickory forest followed by peridomestic areas and seroprevalence rates followed capture data. However, one oak-hickory forest site produced all of the seropositive animals for that habitat type. This particular area is subject to severe flooding and ensuing habitat disturbance could have been more causative of the seroprevalence rates than the habitat type (Eulinger 2003; Ellis et al., 1993). In 2004, focused trapping in oak-hickory forest failed to reproduce the extremely high capture success and seroprevalence seen in 2003 (Cooper, unpublished data).

Another consideration brought to light by capture success data is the prevalence of M. musculus in peridomestic areas. M. musculus captures potentially excluded sigmondotine rodents, especially the habitat generalist P. leucopus from traps, and reduced the number of potentially seropositive animals detected from this habitat type. However, capture of M. musculus in traps set in peridomestic areas is unavoidable. Additionally, no seropositive P. maniculatus or R. megalotis were detected, but they were captured in such small number from one locale that further trapping efforts are essential to evaluate the potential for seropositive P. maniculatus and R. megalotis in northeast Missouri. Also, the serological methodology available did not allow for Microtus samples to be analyzed. Therefore, it is possible that seropositive Microtus exist in northeast Missouri, but were not detected. Therefore, further surveys are needed since Microtus carrying Bloodland Lake hantavirus have already been documented in Missouri, and Prospect Hill virus (another closely related Microtus hantavirus) is known to cause HPS, and P. maniculatus is the vector for Sin Nombre (Sin Nombre strain) Hantavirus, the virus responsible for most HPS cases in the United States.

The presence of Sin Nombre (Blue River-Missouri) in the region is not a cause for panic. It is important to note that seropositive rodents are not necessarily infectious. ELISA analysis tests for the presence of antibodies, not live virus (Mantooth et al., 2001). Therefore, the number of seropositive rodents documented in an area is potentially much greater than the number of infectious ones. However, given the documented presence of Sin Nombre Hantavirus in Missouri and the high fatality rate associated with HPS, physicians and other healthcare providers should be alerted to the possibility of human infection/disease. Public education, and precautionary measures could substantally reduce risk of exposure. Precautions, as outlined by Mills (2002), can be followed to minimize Hantavirus infection potential in areas demonstrated to harbor the virus. Some examples of these precautions include: use of adequate ventilation, wear of surgical masks, and use of disinfectant solutions to reduce aerosolization of dried rodent excretions prior to cleaning outbuildings. Avoidance of rodent bites and rodent proofing of homes also is suggested as a way to prevent infection. These precautions require minor lifestyle modifications and are highly effective at minimizing infection.

Although the results of this project fail to definitely associate Hantavirus seroprevalence to habitat type, significant gains have been made. The known geographic distribution of Hantavirus has been expanded. Sampled rodents provided tissues for subsequent viral sequencing and rodent carcasses have been incorporated into the Truman State Natural History Collection for further study. This endeavor also served not only as an undergraduate research experience, but also as a pilot study for subsequent Master's work looking at the effect of habitat disturbance on P. leucopus hantavirus seroprevalence in oak-hickory forest.

Acknowledgements

The authors would like to thank Truman State University for funding, Dr. Scott Ellis and Dr. Lin Twining for access to data from previous studies, Mary Lou Milazzo for serologic testing, Jessie Harman, Kristen Otten, Kevin Eulinger, Phil Andreas, and Casey Williams for field assistance, The Hooper Family, Truman State University, and Swan Lake National Wildlife refuge for use of their land, and finally Katy Frederick for considerable assistance with figures.

Literature Cited:

Burek, K.A., C.A. Rossi, J.W. Leduc, and T.M. Yuill. 1994. "Serologic and Virologic Evidence of a Prospect Hill-like Hantavirus in Wisconsin and Minnesota." American Journal of Tropical Medicine and Hygiene. Sept; 51(3):286-294.

Centers for Disease Control and Prevention, Special Pathogens Branch, Division of Viral and Ricketsial Disease. "Hantavirus Pulmonary Syndrome by State of Residence-July 13, 2005." Online Case Report Update, Epidemiology of HPS Slide Set, Hantavirus Pulmonary Syndrome. <http://www.cdc.gov/ncidod/diseases/hanta/hps/ noframes/epislides/epis15.htm>. Accessed 14 October 2005.

Childs, J.E., T.G. Ksiazek, C.F. Spiropoulou, J.W. Krebs, S.Morzunov, G.O. Maupin., K.L. Gage, and P.E. Rollin. 1994. "Serologic and Genetic Identification of Peromyscus maniculatus as the Primary Rodent Reservoir for a New Hantavirus in the Southwestern United States." Journal of Infectious Diseases. 169:127-180.

Dietrich, N., S. Pruden, T.G. Ksiazek, S.P. Morzunov, and J.W. Camp. 1997. "A Small Scale Survey of Hantavirus in Mammals from Indiana." Journal of Wildlife Diseases. Oct; 33(4):818-822.

Ellis, L.M. and M.C. Molles, Jr. 1997. "Short Term Effects of Annual Flooding on a Population of Peromyscus leucopus in a Rio Grande Riparian Forest of Central New Mexico." American Midland Naturalist. 138(2):260-268.

Eulinger, K.G. 2003. "Effects of Habitat Disturbance on Small Mammal Community Structure at Swan Lake National Wildlife Refuge." M.S. Thesis, Truman State University, Kirksville, MO.

Hjelle, B., S.W. Lee, W. Song, N. Torrez-Martinez, J.W. Song, R. Yanagihara, I. Gavrilovskaya, and E.R. Mackow. 1995. "Molecular Linkage of Hantavirus Pulmonary Syndrome to the White-footed Mouse, Peromyscus leucopus; Genetic Characterization of the M genome of New York Virus." Journal of Virology. 69, 8137-8141.

Hjelle, B., S.A. Jenison, D.E. Goade, W.B. Green, R.M. Fedderson, and A.A. Scott. 1995b. "Hantaviruses: Clinical, Microbiological, and Epidemiological Aspects. Critical Reviews in Clinical Laboratory Science. 32(5):469-508.

Khan, A.S., Kitsutani, P.T., and Corneli, A.L. 2000. "Hantavirus Pulmonary Syndrome in the Americas: the Early Years." Seminars in Respiratory Critical Care Medicine. 21 (4):313-322.

Langlois, J.P., Fahrig, L., Merriam, G., and Artsob, H. 2001. "Landscape Structure Influences Continental Distribution of Hantavirus in Deer Mice." Landscape Ecology. 16: 255-256.

Lee, P.W., H.L. Amyrx, D.C. Gadjusek, R.T. Yanagihara, D. Goldgaber, and C.J. Gibbs. 1982. "New Hemorrhagic Fever with Renal Syndrome Related Virus in Indigenous Wild Rodents in the United States." Lancet. Dec. 18; 2(8312): 1405.

Mantooth, S.J., M.L. Milazzo, R.D. Bradley, C.L. Hice, G. Ceballos, R.B. Tesh, and C.F. Fulhorst. 2001. "Geographical Distribution of Rodent-associated Hantaviruses in Texas." Journal of Vector Ecology. 26(1):7-14.

Mills, J.N., A. Corneli, J.C. Young, L.E. Garrison, A.S. Khan, and T.G. Ksiazek. 2002. "Hantavirus Pulmonary Syndrome-United States: Updated Recommendations for Risk Reduction." Morbidity and Mortality Weekly Report. Vol 51/ RR 9.

Monroe, M.C., S.P. Morzunov, A.M. Johnson, M.D. Bowen, H. Artsob, T. Yates, C.J. Peters, P.E. Rollin, T.G. Ksiazek, and S.T. Nichol. 1999. "Genetic Diversity and Distribution of Peromyscus-Borne Hantaviruses in North America." Emerging Infectious Diseases. 5(1): 75-86.

Morbidity and Mortality Weekly Report. "Two Cases of Hantavirus Pulmonary Syndrome-Randolph County West Virginia, July 2004." 53(46): 1086-1089.

Morzunov, S.P., H. Feldmann, C.F. Spiropoulou, V.A. Semenova, P.E. Rollin, T.G. Ksiazek, C.J. Peters, and S.T. Nichol. 1995. "A Newly Recognized Virus Associated With a Fatal Case of Hantavirus Pulmonary Syndrome in Louisiana." Journal of Virology. 69, 1980-1983.

Nichol, S.T., C.F. Spiropoulou, S. Morzunov, P.E. Rollin, T.G. Ksaizek, H. Feldmann, A. Sanchez, J. Childs, S. Zaki, and C.J. Peters. 1993. "Genetic Identification of a Hantavirus Associated With an Outbreak of Acute Respiratory Illness." Science. 262, 914-917.

Nichol S.T., B.J. Beaty, R.M. Elliott, R. Goldbach, A. Plyusnin, C.S. Schmaljohn, and R.B. Tesh. 2005. "Family Bunyaviridae." In: Virus Taxonomy, Classification and Nomenclature of Viruses, Eighth Report of the International Committee on Taxonomy of Viruses. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (Eds.), Elsevier Academic Press, 695-716."

Ravkov, E.V., P.E. Rollin, T.G Ksaizek, C.J. Peters, and S.T. Nichol. 1995. "Genetic and Serologic Analysis of Black Creek Canal Virus and its Association with Human Disease and Sigmodon hispidus Infection." Virology. 210, 482-489.

Rawlings, J.A., N. Torrez-Martinez, S.U. Neill, G.M. Moore, B.N. Hicks, S. Pichuantes, A. Nguyen, M. Bharadwaj, and B. Hjelle. 1996. "Cocirculation of Multiple Hantaviruses in Texas, with Characterization of the Small (S) Genome of a Previously Undescribed Virus of Cotton Rats (Sigmodon hispidus)." American Journal of Tropical Medicine and Hygiene. 55,672-679.

Rhodes III, L.V., C. Huang, A.J. Sanchez, S.T. Nichol, S.R. Zaki, T.G. Ksiazek, J.G. Humphreys, J.J. Freeman, and K.R. Knecht. 2000. "Hantavirus Pulmonary Syndrome Associated With Monongahela Virus, Pennsylvania." Emerging Infectious Diseases. 6, 616-621.

Sanchez, A.J., K.D. Abbott, and S.T. Nichol. 2001. "Genetic Identification and Characterization of Limestone Canyon Virus, a Unique Peromyscusborne Hantavirus. Virology. 286, 345-353.

Scharninghausen, J.J., R.M Pitts, J.W. Bickham, D.D. Davis, and J.N. Mills. 1994. "Evidence of Hantavirus Infection in Microtus ochrogaster in St. Louis County, Missouri." Transactions of the Missouri Academy of Science.

Schmaljohn, C. and B. Hjelle. 1997. "Hantaviruses: a Global Disease Problem." Emerging Infectious Diseases. 3, 95-104.

Schwartz, C.W. and E.R. Schwartz. "The Wild Mammals of Missouri." 2nd Ed. Columbia: University of Missouri Press, 2001.

Song, W., N. Torrez-Martinez, W. Irwin, F.J. Harrison, R. Davis, M. Ascher, M. Jay, and B. Hjelle. 1995. "Isla Vista Virus: a Genetically Novel Hantavirus of the California Vole Microtus californicus." Journal of General Virology. Dec; 76(Pt. 12): 3195-9.

Torrez-Martinez, N., W. Song, and B. Hjelle. 1995. "Nucleotide Sequence Analysis of the M Genomic Segment of El Moro Canyon Hantavirus: Antigenic Distinction from Four Corners Hantavirus." Virology. 211, 336-338.

Tsai, T.F., S.P. Bauer, D.R. Sasso, S.G. Whitfield, J.B. McCormick, T.C. Caraway, L. McFarland, H. Bradford, and T. Kurata. 1985. "Serological and Virological Evidence of a Hantaan Virus-Related Enzootic in the United States." Journal of Infectious Disease. 152, 126-136.

Shawna A. Cooper (1,3), M. Scott Burt (1), and Charles F. Fulhorst (2), (1) Truman State University, Division of Science, Kirksville, Missouri 63501. (2) University of Texas Medical Branch, Department of Pathology, Galveston, Texas 77555-0609. (3) Corresponding Author: [e-mail]

Table 1. Summary of principle Hantaviral host associations by rodent
subfamily. Resulting Hantavirus Pulmonary Syndrome (HPS), Hemorrhagic
Fever with Renal Syndrome (HFRS), or pathology unknown (?) are listed
for each virus.

Subfamily             Virus          Disease   Principle Host

Sigmodontinae       Sin Nombre         HPS     Peromyscus maniculatus
                   Monongahela         HPS     Peromyscus maniculatus
                     New York          HPS     Peromyscus leucopus
                  SNV-Blue River        ?      Peromyscus leucopus
                    Limestone
                      Canyon            ?      Peromyscus boylii
                      Bayou            HPS     Oryzomys palustris
                   Black Creek
                      Canal            HPS     Sigmodon hispidus
                     Muleshoe           ?      Sigmodon hispidus
                                               Reithrodontomys
                  El Moro Canon         ?      megalotis

Arvicolinae       Prospect Hill         ?      Microtus pennsylvanicus
                  Bloodland Lake        ?      Microtus ochrogaster
                                               Microtus pennsylvanicus,
                Prospect Hill-like      ?      M.montanus
                                               M. ochrogaster
                    Isla Vista          ?      Microtus califomicus

Murinae               Seoul           HFRS     Rattus norvegicus

Subfamily             Virus          Reference

Sigmodontinae       Sin Nombre       Nichol, S.T. et al., 1993;
                                     Childs, J.E. et al., 1994
                   Monongahela       Rhodes III, L.V. et al., 2000
                     New York        Hjelle, B. et al., 1995
                  SNV-Blue River     Monroe, M. et al., 1999,
                    Limestone
                      Canyon         Sanchez, A.J. et al., 2001
                      Bayou          Morzunov, S.P. et al. 1995
                   Black Creek
                      Canal          Ravkov, E.V. et al., 1995
                     Muleshoe        Rawlings, J.A. et al., 1996
                  El Moro Canon      Torrez-Martinez, N. et al., 1995

Arvicolinae       Prospect Hill      Lee et al., 1982
                  Bloodland Lake     Hjelle, B. et al., 1995b
                Prospect Hill-like   Burek, K.A. et al., 1994
                    Isla Vista       Song, W. et al., 1995

Murinae               Seoul          Tsai, T.F. et al., 1985

Table 2. Capture success per species per habitat type based on a
minimum of 500 trap nights per habitat type. Peridomestic had the
greatest percent trap success, while the highest number of
sigmodontine rodents were captured in Oak-Hickory forest. P.
leucopus were captured in all but one habitat type and accounted
for approximately 77% of total captures.

                Peridomestic   Oak-Hickory    Agriculture-
                                  Forest          Corn

Trap Nights         570            915            500
% Success           9.30           7.10           5.60
CaPtures             53             65             28

Species

Rochrogaster         1              6              3
P.leucopus           21             56             0
P.maniculatus        0              0              19
R.megalotis          0              2              0

                Agriculture-      Native       Disturbed
                    Hay         Grassland      Grassland

Trap Nights         885            500            500
% Success           2.82           1.80           0.60
CaPtures             25             9              3

Species

Rochrogaster         0              0              0
P.leucopus           17             9              3
P.maniculatus        0              0              0
R.megalotis          0              0              0

Table 3. Breakdown of trapping effort by location and habitat type.
Note: All Oak-Hickory forest captures occurred in Chariton County
at Swan Lake Wildlife Refuge. This site also produced 9 of 11
seropositive P. leucopus (Figure 1). Total captures include Mus
musculus, a non-sigmodontine rodent.

County     Locale

Adair      Truman St. Univ. Farm
           Big Creek Conservation
           Sugar Creek Conservation
Chariton   Swan Lake Wildlife Refuge

Schuyler   Greentop (Private Farm)

County     Habitat Type          Trap Nights   Captures   % Success

Adair      Peridomestic              250          33        13.20
           Agriculture-Hay           250           2         0.80
           Disturbed Grassland       500           3         0.60
           Oak Hickory               455           0         0.00
Chariton   Agriculture-Corn          500          28         5.60
           Oak Hickory Forest        460          65        14.13
Schuyler   Peridomestic              320          20         6.25
           Agriculture-Hay           635          23         3.62
           Native Grassland          500           9         1.80
           Total                    3870         183         4.73