Bayou virus detected in non-oryzomyine rodent hosts: an assessment of habitat composition, reservoir community structure, and marsh rice rat social dynamics

In the United States, Bayou virus (BAYV) ranks second only to Sin Nombre virus (SNV) in terms of hantavirus pulmonary syndrome (HPS) incidents, having been confirmed in cases from Texas and Louisiana since its discovery in 1994. This study on BAYV infection among sympatric, non-oryzomyine rodents (“spillover”) in Freeport, TX, is the first to link patterns of hantavirus interspecific spillover with the spatiotemporal ecology of the primary host (marsh rice rat, Oryzomys palustris). Mark-recapture and/or harvest methods were employed from March 2002 through May 2004 in two macrohabitat types. Rodent blood samples were screened for the presence of IgG antibody to BAYV antigen by IFA after which Ab-positive blood, saliva, and urine were analyzed for the presence of viral RNA by nested RT-PCR. From 727 non-oryzomyine captures, five seropositive (but not viral RNA positive) individuals were detected: one each of Baiomys taylori, Peromyscus leucopus, and Reithrodontomys fulvescens; and two Sigmodon hispidus. Spillover hosts were not associated with macrohabitat where O. palustris abundance, density, or seroprevalence was highest. Rather, spillover occurred in the macrohabitat indicative of greater overall disturbance (as indicated by grazing and exotic plant diversity) and overall biodiversity. Spillover occurred during periods of high seroprevalence detected elsewhere within the study region. Spillover locations differed significantly from all other capture locations in terms of percent water, shrub, and grass cover. Although greater habitat and mammal diversity of old-fields may serve to reduce seroprevalence levels by tempering intraspecific contacts between rice rats, greater diversity also may create an ecologically opportunistic setting for BAYV spillover. Impacts of varying levels of disturbance and biodiversity on transmission dynamics represent a vastly uncharacterized component of the evolutionary ecology of hantaviruses. Following human deaths in the southwestern U. S. in 1993 and with the discovery that Sin Nombre virus (SNV; carried by the ubiquitous deermouse, Peromyscus maniculatus) was the causative agent (Nichol et al. 1993), hantaviruses (and Hantavirus Pulmonary Syndrome or HPS) became duly acknowledged throughout the Americas as menacing panzootics. From that time onward, N. American researchers from a variety of scientific disciplines have engaged in numerous transcontinental serosurveys of small mammal communities, focusing mainly on genetic and serologic characterizations, host associations, and the phylogeographic dynamics of SNV (Drebot et al. 2001, Monroe et al. 1999, Spiropoulou et al. 1994). At present, much of what is surmised about the N. American hantavirus assemblage has been extrapolated from information obtained from the initially studied system of SNV and the deermouse, the viral and rodent species to which most HPS cases in the U. S. and Canada have been attributed. Even with an extraordinary compilation of data from hantaviral field and laboratory studies, the modes of transmission, among rodents and from rodent to human, have not been firmly substantiated. Cumulative evidence supports a preponderate transmission dynamic of subcutaneous inoculation of infectious bodily fluids during antagonism between older and perhaps socially dominant males (Glass et al. 1988, Klein 2003). Infection in rodents may be contracted secondarily by inhalation, ingestion, or possibly mucosal absorption of mature virions present in saliva and its aerosols (Orellana 2003); indirect exposure, as rodents navigate through a heavily soiled and virus-contaminated environmental matrix, also has been suggested (Kallio et al. 2006, Sauvage et al. 2003). Indirect transmission of this nature could have far-reaching consequences, particularly among communities with species that scent mark their territorial boundaries with urine and/or feces, and among individuals that engage in olfactory exploration while attempting to secure a breeding home range. The durability of hantaviruses outside their mammalian hosts is unknown, although Hutchinson et al. (1998) and Kallio et al. (2006) have shown support for external survivability of Black Creek Canal virus (BCCV) and Puumala virus (PUUV), respectively. Comparably virulent RNA viruses transmitted normally by some form of social or physical contact have evolved the capacity for prolonged survival in liquid media, the soil strata, or forest litter, such as rabies virus and various arenaviruses and enteroviruses (Garnett and Antia 1994). It is widely believed that hantaviruses cause no discernible, deleterious effects in their rodent hosts with respect to fecundity or longevity (Bernshtein et al. 1999, Schmaljohn and Hjelle 1997), despite studies which entertain a re-evaluation of the reigning paradigm of the benign nature of hantaviral infection in rodents (Douglass et al. 2001, Kuenzi et al. 1999). Transmission of hantavirus from specific (primary) hosts to non-specific secondary (reservoir) hosts (“spillover”) is speculated to occur frequently among natural populations of rodents living in sympatry or syntopy (Monroe et al. 1999), particularly during periods of high rodent population density (Mills et al. 1997) and/or seroprevalence; these conditions also are believed to act synergistically to accelerate viral spreading throughout the rodent community due to increased rodent-to-rodent contacts (Hjelle and Yates 2001). Ironically, compelling evidence has not been produced for a clear covariation between rodent host densities and seroconversion incidence (Abbott et al. 1999, Biggs et al. 2000). Hantavirus spillover in nature is perceived as inconsequentially common for the most part because non-primary host cells are assumed to be incompatible with viral colonization-induced persistence (precluded by the ancient virus-carrier union of coevolutionary specificity and microadaptation). Therefore, spillover hosts may not be hosts at all or perhaps fleeting hosts at best, as their immune systems expunge the viruses rapidly; thus with regards to the cycle of viral trafficking and maintenance within rodent and human communities, their expected contribution should be insignificant. No information is available on the potential impacts of non-primary hosts functioning minimally as short-term transporters and translocaters of hantaviruses. However, these roles are worthy of investigation, as there are several examples of how prolonged association of hantavirus infection in a secondary host can lead eventually to interspecific host switching. For these reasons, the importance of spillover hosts, and the elucidation of the conditions under which spillover occurs, should not be underestimated. In North America to date, no published works have investigated hantavirus spillover in rodents explicitly, to attempt quantification of relative frequencies of occurrence, to characterize possible spatiotemporal reservoir-habitat associations, or to assess possible impacts on transmission rates between rodents and from rodents to humans or alterations in virus evolution. Czech Republic researchers have produced genetic evidence for Dobrava virus (DOBV) spillover from the yellow-necked field mouse (Apodemus flavicollis) to other rodents (Weidmann et al. 2005) and in Sweden, Klingström et al. (2002) have demonstrated secondary host infection of PUUV in artificially and naturally infected rodents. The previous two examples notwithstanding, mostly known information about hantavirus spillover (among both wild-trapped and lab-reared rodents) is anecdotal, reported sporadically as ancillary data from studies with widely varied emphases (Abbott et al. 1999, Childs et al. 1994, Hjelle and Yates 2001, Jay et al. 1997, Kuenzi et al. 2001, Levis et al. 1998, Mills et al. 1997; 1999, Rawlings et al. 1996, Rhodes et al. 2000, Rowe et al. 1995, Schmaljohn and Hjelle 1997, Ulrich et al. 2002). As part of a broader ecological study of BAYV and the marsh rice rat (McIntyre et al. 2005), our objectives here were to detect and describe spillover hosts, and to ecologically characterize spillover sites in comparison with non-spillover sites at our study location. Moreover, our intent was to ascertain how rice rat demographic or behavioral features, host community structure, or specific habitat variables might predict areas where secondary host infection is likely to occur. Rodent trapping and habitat assessment were conducted seasonally at the Peach Point Wildlife Management Area (PPWMA) (UTM: 15-3202562-262435) in Brazoria County, TX, from March 2002 through May 2004. Representative of the Gulf Coast Prairies and Marshes Ecoregion, PPWMA is located approximately 100 km south of Houston, encompasses 4174.5 ha, and is bordered southeasterly by the Gulf Coast Intracoastal Waterway (GCIW). Topographically, the landscape is relatively flat and low (0–5 m ASL) with clay soils, and is composed of low-lying assemblages of brackish to saline coastal prairies, grading farther inland to upland habitats of freshwater marshes and old-fields with some trees. The area experiences episodic tropical storms, resulting in inundation of areas near the GCIW. Precipitation occurs throughout the year (with 60% falling between April and September), and average precipitation is 133.35 cm/yr (data from the National Oceanic and Atmospheric Administration Freeport 2NW weather station, located ∼10 km from PPWMA; http://www.noaa.gov/). Average high temperatures range from 18° C in winter to 33° C in summer; average annual lows are above freezing (8° C) even in winter. Field collection protocols were approved by the Texas Tech University Animal Care and Use Committee (permit #01134BX) prior to the onset of this study. Trapping and sampling procedures were sanctioned by, and scientific collection permits were secured from, the Texas Parks and Wildlife Department (permits #APR-0498-944 and #SPR-0504-381). To characterize the rodent community, a pilot study was conducted in mid-March 2002, when species diversity, distributions, and antibody status of rodents were determined using standard small mammal capture and harvest methods (Jones et al. 1996, Mills et al. 1995a). From those data, two simultaneous yet spatially independent trapping designs were implemented in May 2002. Rodents were live-trapped on four capture-mark-release-recapture grids (each ∼7100 m2, ca. 100 traps each) in both macrohabitat types (two in coastal prairie, two in old-field) for four to six consecutive nights per each of four seasons (mid-March, late May, late August, mid-December). Grid shapes, dimensions, and trap numbers varied slightly due to waterline constraints. Grids were separated by >1 km to demarcate individual rodent populations. Specimens were live-captured using Sherman 7.8 × 9.3 × 23.5 cm folding galvanized aluminum traps (H. B. Sherman Traps, Inc., Tallahassee, FL) placed singly on terra firma (exception: affixed to floating rafts on Grids 3 and 4 when inundated; see Abuzeineh et al. 2007 for descriptions) at 10-m intervals (Jones et al. 1996). Slightly before dusk, traps were baited with rolled oats and peanut butter. Traps were checked immediately after dawn to minimize stress-induced deaths resulting from hypothermia, starvation, and/or dehydration, and traps remained closed during the day to avoid diurnal capture mortalities. New plastic were to each and time was to a while each at the of Rodents were by a or by a or by Inc., for each individual rodent capture status or its trap station, a and status or or or also were the and of and with physical were using a system cells and saliva were with a and placed immediately a of and an of a urine when was from the and in the as a a blood of several was from the and to a after which the was at the of was and samples were on while in the and samples were within liquid during trapping seasons were and to in and and infection procedures for and of as as human were employed (Mills et al. each all contact were with a and/or were in the at the in an to the were in locations on the PPWMA that were spatially from of the four grids in terms of plant species of with traps m were for four to six of varied seasonally and disturbance and area was to the at each where a rodent was plastic were to traps rodents to a At a within the all were from the and in a by permits and The was between by a was for in a the was with all of liquid Following blood each was as a standard et al. 1996). were during all of and (Mills et al. To a of was for each and all and contact were with a between to their and traps were for in a for with water, and placed in the and for of liquid and for using rodent and were conducted at the and to and The were and by et al. 2003). and cells on a were as To detect of an of from each rodent were to a of the antigen were for at C in a with saline for and with were of IgG and Inc., were were for and as with in were under a for presence of To antibody antibody samples were with a and each was as samples from rodents confirmed to have IgG and samples from confirmed rodents) were for RNA from Ab-positive and rodent was and by nested using protocols et al. 1995, 2003). of the methods can be in et al. was at of and 3 m in on each trap and for and percent of of plant and of protocols in et al. habitat was for a of The were to a From the ecological two at m and at were from the due to and one of was because of was using habitat as independent variables to spillover sites could be from non-spillover sites other capture each a for all traps for the of the study. For two a the the second only permits the to be by of variables with the were as of was to assess or not the spillover sites differed significantly from the non-spillover To avoid the of of and and levels of were by 1997) using The and were using all trap locations no capture and for spillover sites non-spillover to the of spillover to all other trap no capture were from the capture were were using in In this and rodent species differed between the two macrohabitat types. coastal was in terms of both and the of each by and average of plant and small mammal as as the dominant plant terms of percent the study and rodent and other the of grids and the of grids 3 and 4 and the between the two the dominant rodent species by small mammal and plant species and from Grid 4 the study and in both macrohabitat of small mammal species varied with BAYV seroprevalence levels In habitat the of small mammal species was the of species in coastal habitat of seroprevalence in were the levels in coastal habitat and of antibody and of known small mammal species in and in coastal habitat at the Brazoria County, TX, From approximately trap non-oryzomyine rodents Reithrodontomys harvest Sigmodon Baiomys taylori, Peromyscus leucopus, were and on the four from approximately trap an were from the fulvescens; S. B. IgG was detected in S. B. and host rodents for the presence of of the are shown in of the trap (as by the habitat where rodents were to the in the represent where rodents were has been (with non-spillover capture by the to of the of between the five spillover locations and all other capture locations The where two spillover hosts were at a trap by ecological variables for both spillover are the The between the ecological variables and the that the habitat to spillover sites from non-spillover sites are percent at m at m and at 3 m and percent at m and at 3 m percent grass at m at m and at 3 m are with spillover rodents. on the spillover sites differed significantly from all other capture sites of the for capture sites as is all capture types other spillover. the ecological of spillover as where of the the on an ecologically area where two spillover hosts were between the and habitat variables for the habitat variables are as Average plant in cm 3 3 of plant species m 3 m hosts were detected in of the trapping of spillover occurred during 3 of the 4 periods of precipitation five spillover rodents were on the 2002, or from Grid and no spillover was detected on Grid or Grids 3 and 4 Spillover hosts one and one In March 2002, two S. were from the In March one B. was from a and one was and on Grid in March on Grid one was and only to be five in at which time seroconversion was this only one seropositive rice rat was on Grid initially in May this rodent was in the trapping trap placed in the of a in this was virus in blood and saliva both was spillover rodents on Grid were within m and m of the rice rat, and both spillover rodents were within m and m of the Grid was the only a of in the of and rice (data not from all and species of the in this study. Although of Oryzomys and were approximately and the of the to trapping was not the species of the of captures, for of the and varied by macrohabitat and (McIntyre et al. rice rat and seroprevalence were in individuals per and in coastal individuals per and BAYV interspecific spillover to occur when primary host not when primary host abundance, is Moreover, spillover not occur where rice rat is 3 and For no spillover occurred on the or the grids during May or 2002, despite relatively high capture rates of O. palustris of rodent community of the marsh rice rat, Oryzomys palustris and in rice rat represent species with of for all 4 grids and all by trapping trapping when spillover was our study the small mammal community is of one one two and one data not and one habitats the other species occur in habitats with greater and 1994). The most in this coastal Oryzomys is known to its primary of to et al. on and plant and also and and At of the the rice rat may of from the et al. in the of O. palustris habitat and with populations of S. and other transmitted mammalian hantaviruses a for both physical contact and in their rodent hosts et al. 2002, et al. see also Klein 2003). infected by virus several for transmission such as increased and with a status (Glass et al. 1988, Klein et al. is not the only between infected and rice rat with their rice are and have (McIntyre et in for are in and home range seropositive males (McIntyre et in In some and are status of et al. because the these physical the likely the should be to home and not in for periods of time from their frequently see Abuzeineh et al. Therefore, an system of within populations be to this could occur during prolonged periods of high population density and home range which can lead to or perhaps when a population relatively for a in which both and might roles in potential between rodents. In our Grid rice rat and although of each and were relative population could a in the of and BAYV spillover. assessment of the rice rat in Texas not support the that hantaviral spillover is common among species of rodents. Rather, the data a relatively low incidence of secondary host infection even in the rat a non-oryzomyine ecologically and to the rice rat and of the rodent our data not support to the for rodent density, high primary host This is not to that under ecological or host community or or in be is that to BAYV infection an to and that there was no in non-primary host The population of the dynamics of the virus both within and between host rodents. host populations present as for hantavirus survival in terms of in density, and Moreover, because individual host immune hantaviruses be to to the host before the host persistence or In other viral host specificity should be a common to host and secure hantavirus infection and thus and of the most likely is by a variety of and behavioral host rodent hosts be the most small mammal in their community, the to virus throughout their and engage in physical contact with other rodents. to the host specificity can lead to high of the primary host population and the virus is to in species in some of external To reduce the of in rodent some hantaviruses may have been to a broader of mammalian RNA viruses hantaviruses have high and host both of which not only to environmental or host behavioral also infection of a host by to the host et al. have investigated spillover as to and host from primary hosts of the and New Monroe et al. 1999, Rowe et al. 1995, Ulrich et al. 2002). to spillover hosts are believed to have no on the or maintenance of hantaviruses or their despite numerous examples of how prolonged spillover can lead to host between species of et al. 2002, Levis et al. 1998, 1999). some secondary hosts to a in host intraspecific to be the of BAYV transmission in the and and longevity and in the rice rat could of BAYV within the rodent community as as to ecological and can create a setting for interspecific spillover from rice rat of percent during low shrub, and grass may be habitat for the of males may habitat of and where also may infection to individuals of other and behavioral of (McIntyre et in for how from the rice rat may in the of other or sites or could by which the virus is within and between the et al. of Bayou by O. palustris for to several might a in BAYV transmission in where and conditions breeding in the rice rat how may not hantavirus spillover in rodents occur by is an for survival a to in the primary species is As with or ecological can be Although is that are the primary for hantavirus transmission to the and host even spillover may have of hantavirus spillover may to be in in support for this was by the of Texas and to and were by a a and an of are of the Texas Parks and Wildlife and the Peach Point Wildlife Management Area and and the of for their with and the Department of and for and also the for and Jay and to and one

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