Habitat, species richness and hantaviruses of sigmodontine rodents within the Interior Atlantic Forest, Paraguay

Abstract

Four of the nine sigmodontine tribes have species that serve as reservoirs of rodent-borne hantaviruses (RBO-HV), few have been studied in any depth. Several viruses have been associated with human cases of hantavirus pulmonary syndrome often through peridomestic exposure. Jabora (JABV) and Juquitiba (JUQV), harbored by Akodon montensis and Oligoryzomys nigripes, respectively, are endemic and sympatric in the Reserva Natural de Bosque Mbaracayú (RNBM), Paraguay, a protected area of the Interior Atlantic Forest. Rodent communities were surveyed along a 30 km stretch of the RNBM in eight vegetation classifications (Low, High, Bamboo, Riparian and Liana Forests, Bamboo Understory, Cerrado, and Meadow/Grasslands). We collected 417 rodents from which 11 species were identified; Akodon montensis was the predominant species (72%; 95%CI: 64.7%-76.3%), followed by Hylaeamys megacephalus (15% (11.2%-18.2%)) and Oligoryzomys nigripes (9% (6.6%-12.4%)). We examined the statistical associations among habitat (vegetation class) type, rodent species diversity, population structure (age, sex, and weight), and prevalence of RBO-HV antibody and/or viral RNA (Ab/RNA) or characteristic Leishmania tail lesions. Ab/RNA positive rodents were not observed in Cerrado and Low Forest. A. montensis had an overall Ab/RNA prevalence of 7.7% (4.9%-11.3%) and O. nigripes had an overall prevalence of 8.6% (1.8%-23.1%). For A. montensis, the odds of being Ab/RNA positive in High Forest was 3.73 times of the other habitats combined. There was no significant difference among age classes in the proportion of Ab/RNA positive rodents overall (p = 0.66), however, all 11 RNA-positive individuals were adult. Sex and habitat had independent prognostic value for hantaviral Ab/RNA in the study population; age, presence of tail scar/lesion (19% of the rodents) and weight did not. Adjusting for habitat, female rodents had less risk of becoming infected. Importantly, these data suggest habitat preferences of two sympatric rodent reservoirs for two endemic hantaviruses and the importance of including habitat in models of species diversity and habitat fragmentation.

Mixed Effects of Habitat Degradation and Resources on Hantaviruses in Sympatric Wild Rodent Reservoirs within a Neotropical Forest

“…The MFBR comprises the Interior Atlantic Forest, which formerly covered large portions of Southern Brazil, Northeastern Argentina, and Eastern Paraguay. Previously, we surveyed 21 sites across the MFBR ( Figure 1 A) for rodents and measured the presence of antibodies to hantaviral antigens as well as the presence and sequencing of hantaviral RNA [ 37 ]. Based on this information, we extensively assessed vegetation and habitat disturbance to select three pairs of 12 × 12 sampling grids ( Supplemental Text, Figure S1 ).…”

“…An indirect immunofluorescence assay (IFA) was used to screen blood samples for the presence of antibodies cross-reactive with ANDV grown in Vero E6 cells on microscope spot slides as described previously [ 42 ]. We have previously demonstrated the sympatry of Jabora virus (JABV) and Juquitiba virus (JUQV) in this study site in their reservoir hosts, Akodon montensis and Oligoryzomys nigripes , respectively [ 35 , 37 ]. As hantaviruses cause a chronic infection of rodents, we use seroprevalence as a measure of hantaviral activity, as is common in these types of field studies [ 1 , 15 ].…”

“…In the neotropical forests of South America, it is clear that the outcome depends primarily on the ecology of rodent–virus interactions within their immediate local environment. We have identified and characterized an ecosystem in a neotropical forest in Paraguay where Akodon montensis and Oligoryzomys nigripes , two sigmodontine rodents, are the primary reservoirs of Jabora and Juquitiba viruses, respectively [ 34 , 35 , 36 , 37 , 38 ]. This system allows us to investigate ecological factors that influence hantavirus prevalence and test whether those factors are species-specific.…”

“…As we have intensively characterized landscape effects on rodent dynamics within this habitat [ 17 , 34 , 35 , 36 , 37 , 38 , 39 , 40 , 41 , 42 ], we could control for landscape- and habitat-specific effects which may otherwise confound studies in the neotropics [ 14 , 16 , 37 , 39 , 43 , 44 ]. This allowed us to control for (and test) the previous observations that habitat degradation may be the primary driver of hantavirus prevalence in neotropical habitats [ 36 , 37 , 40 , 41 , 42 ]. More specifically, we have previously shown that these two rodent reservoir species have fundamentally different microhabitat requirements, defined by vegetation characteristics at a given trap station, yet are sympatric on a marginally larger spatial scale [ 36 , 37 ].…”

“…This allowed us to control for (and test) the previous observations that habitat degradation may be the primary driver of hantavirus prevalence in neotropical habitats [ 36 , 37 , 40 , 41 , 42 ]. More specifically, we have previously shown that these two rodent reservoir species have fundamentally different microhabitat requirements, defined by vegetation characteristics at a given trap station, yet are sympatric on a marginally larger spatial scale [ 36 , 37 ]. This enabled us to test whether these changes in resource augmentation affected fine-scale habitat associations of rodent reservoir abundance and hantavirus prevalence as well as our previously defined larger scale associations of habitat degradation [ 17 , 40 ].…”