Spatial clusters, temporal behavior, and risk factors analysis of rabies in livestock in Ecuador.

Rabies, a globally distributed and highly lethal zoonotic neglected tropical disease, has a significant impact in South America. In Ecuador, animal rabies cases are primarily linked to livestock, and hematophagous bats play a crucial role in disease transmission. This study aims to identify temporal trends, spatial patterns, and risk factors for animal rabies in Ecuador between 2014 and 2019. Epidemiological survey reports from the official Animal Rabies Surveillance Program of the Phyto and Zoosanitary Regulation and Control Agency of Ecuador (AGROCALIDAD) were used. The Animal Rabies Surveillance Program from AGROCALIDAD consists of an official passive surveillance program that receives reports from farmers or individuals (both trained or untrained) who have observed animals with neurological clinical signs and lesions compatible with bat bites, or who have seen or captured bats on their farms or houses. Once this report is made, AGROCALIDAD personnel is sent for field inspection, having to confirm the suspicion of rabies based on farm conditions and compatibility of signs. AGROCALIDAD personnel collect samples from all suspicious animals, which are further processed and analyzed using the Direct Fluorescent Antibody (DFA) test for rabies confirmatory diagnosis. In this case, study data comprised 846 bovine farms (with intra-farm sample sizes ranging from 1 to 16 samples) located in different ecoregions of Ecuador; out of these, 397 (46.93%) farms tested positive for animal rabies, revealing six statistically significant spatial clusters. Among these clusters, three high-risk areas were identified in the southeast of Ecuador. Seasonality was confirmed by the Ljung-Box test for both the number of cases (p < 0.001) and the positivity rate (p < 0.001). The Pacific Coastal lowlands and Sierra regions showed a lower risk of positivity compared to Amazonia (OR = 0.529; 95% CI = 0.318 - 0.883; p = 0.015 and OR = 0.633; 95% CI = 0.410 - 0.977; p = 0.039, respectively). The breeding of non-bovine animal species demonstrated a lower risk of positivity to animal rabies when compared to bovine (OR = 0.145; 95% CI = 0.062 - 0.339; p < 0.001). Similarly, older animals exhibited a lower risk (OR = 0.974; 95% CI = 0.967 - 0.981; p < 0.001). Rainfall during the rainy season was also found to decrease the risk of positivity to animal rabies (OR = 0.996; 95% CI = 0.995 - 0.998; p < 0.001). This study underscores the significance of strengthening the national surveillance program for the prevention and control of animal rabies in Ecuador and other countries facing similar epidemiological, social, and geographical circumstances.

Association between anthropization and rodent reservoirs of zoonotic pathogens in Northwestern Mexico.

The world is facing a major pulse of ecological and social changes that may favor the risk of zoonotic outbreaks. Such risk facilitation may occur through the modification of the host's community diversity and structure, leading to an increase in pathogen reservoirs and the contact rate between these reservoirs and humans. Here, we examined whether anthropization alters the relative abundance and richness of zoonotic reservoir and non-reservoir rodents in three Socio-Ecological Systems. We hypothesized that anthropization increases the relative abundance and richness of rodent reservoirs while decreasing non-reservoir species. We first developed an Anthropization index based on 15 quantitative socio-ecological variables classified into five groups: 1) Vegetation type, 2) Urbanization degree, 3) Water quality, 4) Potential contaminant sources, and 5) Others. We then monitored rodent communities in three regions of Northwestern Mexico (Baja California, Chihuahua, and Sonora). A total of 683 rodents of 14 genera and 27 species were captured, nine of which have been identified as reservoirs of zoonotic pathogens (359 individuals, 53%). In all regions, we found that as anthropization increased, the relative abundance of reservoir rodents increased; in contrast, the relative abundance of non-reservoir rodents decreased. In Sonora, reservoir richness increased with increasing anthropization, while in Baja California and Chihuahua non-reservoir richness decreased as anthropization increased. We also found a significant positive relationship between the anthropization degree and the abundance of house mice (Mus musculus) and deer mice (Peromyscus maniculatus), the most abundant reservoir species in the study. These findings support the hypothesis that reservoir species of zoonotic pathogens increase their abundance in disturbed environments, which may increase the risk of pathogen exposure to humans, while anthropization creates an environmental filtering that promotes the local extinction of non-reservoir species.

Molecular detection and characterization of Bartonella spp. in rodents from central and southern Chile, with emphasis on introduced rats (Rattus spp.).

Bartonella spp. was screened in 155 rodents from Chile, mainly the invasive rats Rattus norvegicus and Rattus rattus. A total of 155 spleen and 50 blood samples were analyzed through real-time PCR for Bartonella spp. (nuoG gene). Positive samples were subjected to amplification of fragment of loci gltA, rpoB and ITS by conventional PCR (cPCR). Overall, 43 spleen samples (27.7%) and 6 rodent blood samples (12%) were positive for nuoG-Bartonella spp. Positive samples were found in R. norvegicus, R. rattus, Abrothrix olivacea and Oligoryzomys longicaudatus. Bartonella spp. DNA was amplified by cPCR in 16 samples, resulting in 21 sequences (6 gltA, 5 ITS and 10 rpoB). Sequencing and phylogenic analyses identified genotypes from Rattus spp., potentially belonging to Bartonella coopersplainsensis, Bartonella henselae, Bartonella tribocorum, and an undescribed Bartonella sp. From native rodents, one sequence was identified, being related B. machadoae. In conclusion, this work describes diverse and potentially zoonotic Bartonella spp. genotypes in Rattus spp. Additionally, this is the first report of Bartonella in O. longicaudatus, including a potentially novel Bartonella genotype or species.

Molecular surveillance of potential SARS-CoV-2 reservoir hosts in wildlife rehabilitation centers.

BACKGROUND: The COVID-19 pandemic, caused by SARS-CoV-2 infection, has become the most devastating zoonotic event in recent times, with negative impacts on both human and animal welfare as well as on the global economy. Although SARS-CoV-2 is considered a human virus, it likely emerged from animals, and it can infect both domestic and wild animals. This constitutes a risk for human and animal health including wildlife with evidence of SARS-CoV-2 horizontal transmission back and forth between humans and wild animals. AIM: Molecular surveillance in different wildlife rehabilitation centers and wildlife associated institutions in Chile, which are critical points of animal-human interaction and wildlife conservation, especially since the aim of wildlife rehabilitation centers is to reintroduce animals to their original habitat. MATERIALS AND METHODS: The survey was conducted in six WRCs and three wildlife associated institutions. A total of 185 samples were obtained from 83 individuals belonging to 15 different species, including vulnerable and endangered species. Each specimen was sampled with two different swabs: one oropharyngeal or nasopharyngeal according to the nostril diameter, and/or a second rectal sample. RNA was extracted from the samples and two different molecular assays were performed: first, a conventional RT-PCR with pan-coronavirus primers and a second SARS-CoV-2 qPCR targeting the N and S genes. RESULTS: All 185 samples were negative for SARS-CoV-2. CLINICAL RELEVANCE: This study constitutes the first report on the surveillance of SARS-CoV-2 from wildlife treated in rehabilitation centers in Chile, and supports the biosafety procedures adopted in those centers.

Cryptosporidium spp. and Giardia spp. in wild rodents: using occupancy models to estimate drivers of occurrence and prevalence in native forest and exotic Pinus radiata plantations from Central Chile.

The conversion of native forest to forestry plantations is a worldwide practice, affecting biodiversity and host-parasite interactions. One of the most common timber plantations in the world are monocultures of Monterey pine (Pinus radiata). Using occupancy models, we analyzed the occurrence and prevalence of Cryptosporidium spp. oocysts and Giardia spp. cysts in fecal samples of wild rodents from a landscape dominated by extensive Monterey pine plantations in central Chile. We aimed to assess drivers of parasite infection such as habitat type, abundance of rodent hosts, species richness, and season. Small mammals were sampled seasonally for two years in three habitat types: native forests, adult pine plantations and young pine plantations. A total of 1091 fecal samples from seven small mammal species were analyzed by coprological analysis. Occurrence probability of Cryptosporidium spp. and Giardia spp. was similar for the most abundant rodent species (Abrothrix longipilis, A. olivacea, and Oligoryzomys longicaudatus) and for all habitat types. For Cryptosporidium spp., variation in prevalence was mostly explained by season with higher prevalence during winter season and lower during spring. For Giardia spp., the prevalence was significantly higher in young pine plantations, followed by adult pine plantations and native forests. In addition, higher prevalence of Giardia spp. was associated with lower host richness, suggesting a possible dilution effect. Our findings reveal that Monterey pine plantations increase Giardia spp. transmission among rodents, but has no clear effect on Cryptosporidium spp., providing evidence that the impact of land use on parasitism can be idiosyncratic. Since both parasites have zoonotic potential, our findings may be useful for land use planning and management considering health issues.

Activity patterns and interactions of rodents in an assemblage composed by native species and the introduced black rat: implications for pathogen transmission.

Background: The degree of temporal overlap between sympatric wild hosts species and their behavioral interactions can be highly relevant to the transmission of pathogens. However, this topic has been scantly addressed. Furthermore, temporal overlap and interactions within an assemblage of wild rodents composed of native and introduced species have been rarely discussed worldwide. We assessed the nocturnal activity patterns and interactions between rodent taxa of an assemblage consisting of native species (Oligoryzomys longicaudatus, Abrothrix hirta, and Abrothrix olivaceus) and the introduced black rat (Rattus rattus) in a temperate forest from southern Chile. All rodent species in this study are known hosts for various zoonotic pathogens. Results: We found a high nocturnal temporal overlap within the rodent assemblage. However, pairwise comparisons of temporal activity patterns indicated significant differences among all taxa. Rattus rattus showed aggressive behaviors against all native rodents more frequently than against their conspecifics. As for native rodents, agonistic behaviors were the most common interactions between individuals of the same taxon and between individuals of different taxa (O. longicaudatus vs Abrothrix spp.). Conclusions: Our findings reveal several interactions among rodent taxa that may have implications for pathogens such as hantaviruses, Leptospira spp., and vector-borne pathogens. Furthermore, their transmission may be facilitated by the temporal overlap observed between rodent taxa. Supplementary Information: The online version contains supplementary material available at 10.1186/s40850-022-00152-7.

Land-use change and rodent-borne diseases: hazards on the shared socioeconomic pathways.

Land-use change has a direct impact on species survival and reproduction, altering their spatio-temporal distributions. It acts as a selective force that favours the abundance and diversity of reservoir hosts and affects host-pathogen dynamics and prevalence. This has led to land-use change being a significant driver of infectious diseases emergence. Here, we predict the presence of rodent taxa and map the zoonotic hazard (potential sources of harm) from rodent-borne diseases in the short and long term (2025 and 2050). The study considers three different land-use scenarios based on the shared socioeconomic pathways narratives (SSPs): sustainable (SSP1-Representative Concentration Pathway (RCP) 2.6), fossil-fuelled development (SSP5-RCP 8.5) and deepening inequality (SSP4-RCP 6.0). We found that cropland expansion into forest and pasture may increase zoonotic hazards in areas with high rodent-species diversity. Nevertheless, a future sustainable scenario may not always reduce hazards. All scenarios presented high heterogeneity in zoonotic hazard, with high-income countries having the lowest hazard range. The SSPs narratives suggest that opening borders and reducing cropland expansion are critical to mitigate current and future zoonotic hazards globally, particularly in middle- and low-income economies. Our study advances previous efforts to anticipate the emergence of zoonotic diseases by integrating past, present and future information to guide surveillance and mitigation of zoonotic hazards at the regional and local scale. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

Intestinal Helminths in Wild Rodents from Native Forest and Exotic Pine Plantations (Pinus radiata) in Central Chile.

Native forests have been replaced by forestry plantations worldwide, impacting biodiversity. However, the effect of this anthropogenic land-use change on parasitism is poorly understood. One of the most important land-use change in Chile is the replacement of native forests by Monterey pine (Pinus radiata) plantations. In this study, we analyzed the parasitism (presence and prevalence) of intestinal helminths from fecal samples of wild rodents in three habitat types: native forests and adult and young pine plantations in central Chile. Small mammals were sampled seasonally for two years, and a total of 1091 fecal samples from seven small mammal species were analyzed using coprological analysis. We found several helminth families and genera, some of them potentially zoonotic. In addition, new rodent-parasite associations were reported for the first time. The overall helminth prevalence was 16.95%, and an effect of habitat type on prevalence was not observed. Other factors were more relevant for prevalence such rodent species for Hymenolepis sp. and season for Physaloptera sp. Our findings indicate that pine plantations do not increase helminth prevalence in rodents compared to native forests.

Exotic Pinus radiata Plantations do not Increase Andes Hantavirus Prevalence in Rodents.

Andes south virus (ANDV) is the etiologic agent of hantavirus cardiopulmonary syndrome (HCPS) in Chile and southern Argentina. Farm and forestry workers have been identified as a group at high risk of acquiring HCPS caused by ANDV due to their close exposure to rodents or their secretions in rural areas. Therefore, investigation on the effect of landscape composition on ANDV in wild rodents becomes relevant for disease prevention and control. In this study, we analyzed the influence of Monterey pine (Pinus radiata) plantations, an important monoculture in the global forest industry, on small mammal assemblage and on ANDV seroprevalence and abundance of seropositive rodents from central Chile. Small mammals were sampled seasonally during 2 years in native forests, adult pine plantations and young pine plantations. A total of 1630 samples from seven rodent species were analyzed for antibody detection. ANDV seroprevalence and abundance of seropositive rodents were significantly higher in the native forest compared to pine plantations. Furthermore, Monterey pine plantations decrease the abundance and relative abundance of Oligoryzomys longicaudatus (the principal reservoir of ANDV) and do not change sex ratio and distribution of age classes of this rodent species, which are variables that are important for ANDV transmission. Our findings indicate that Monterey pine plantations would not pose a higher risk of human exposure to ANDV compared to the temperate native forest. Our results can be useful for hantavirus risks assessment in human-dominated areas where ANDV is endemic.

Drivers of flea (Siphonaptera) community structure in sympatric wild carnivores in northwestern Mexico.

Host identity, habitat type, season, and interspecific interactions were investigated as determinants of the community structure of fleas on wild carnivores in northwestern Mexico. A total of 540 fleas belonging to seven species was collected from 64 wild carnivores belonging to eight species. We found that the abundances of some flea species are explained by season and host identity. Pulex irritans and Echidnophaga gallinacea abundances were significantly higher in spring than in fall season. Flea communities on carnivore hosts revealed three clusters with a high degree of similarity within each group that was explained by the flea dominance of E. gallinacea, P. simulans, and P. irritans across host identity. Flea abundances did not differ statistically among habitat types. Finally, we found a negative correlation between the abundances of three flea species within wild carnivore hosts. Individual hosts with high loads of P. simulans males usually had significantly lower loads of P. irritans males or tend to have lower loads of E. gallinacea fleas and vice-versa. Additionally, the logistic regression model showed that the presence of P. simulans males is more likely to occur in wild carnivore hosts in which P. irritans males are absent and vice-versa. These results suggest that there is an apparent competitive exclusion among fleas on wild carnivores. The study of flea community structure on wild carnivores is important to identify the potential flea vectors for infectious diseases and provide information needed to design programs for human health and wildlife conservation.

Species Identity Supersedes the Dilution Effect Concerning Hantavirus Prevalence at Sites across Texas and México.

Recent models suggest a relationship exists between community diversity and pathogen prevalence, the proportion of individuals in a population that are infected by a pathogen, with most inferences tied to assemblage structure. Two contrasting outcomes of this relationship have been proposed: the "dilution effect" and the "amplification effect." Small mammal assemblage structure in disturbed habitats often differs from assemblages in sylvan environments, and hantavirus prevalence is often negatively correlated with habitats containing high species diversity via dilution effect dynamics. As species richness increases, prevalence of infection often is decreased. However, anthropogenic changes to sylvan landscapes have been shown to decrease species richness and/or increase phylogenetic similarities within assemblages. Between January 2011 and January 2016, we captured and tested 2406 individual small mammals for hantavirus antibodies at 20 sites across Texas and México and compared differences in hantavirus seroprevalence, species composition, and assemblage structure between sylvan and disturbed habitats. We found 313 small mammals positive for antibodies against hantaviruses, evincing an overall prevalence of 9.7% across all sites. In total, 40 species of small mammals were identified comprising 2 taxonomic orders (Rodentia and Eulipotyphla). By sampling both habitat types concurrently, we were able to make real-world inferences into the efficacy of dilution effect theory in terms of hantavirus ecology. Our hypothesis predicting greater species richness higher in sylvan habitats compared to disturbed areas was not supported, suggesting the characteristics of assemblage structure do not adhere to current conceptions of species richness negatively influencing prevalence via a dilution effect.

Molecular Survey of Bartonella Species and Yersinia pestis in Rodent Fleas (Siphonaptera) From Chihuahua, Mexico.

Rodent fleas from northwestern Chihuahua, Mexico, were analyzed for the presence of Bartonella and Yersinia pestis. In total, 760 fleas belonging to 10 species were tested with multiplex polymerase chain reaction analysis targeting the gltA (338-bp) and pla genes (478-bp) of Bartonella and Y. pestis, respectively. Although none was positive for Y. pestis, 307 fleas were infected with Bartonella spp., resulting in an overall prevalence of 40.4%. A logistic regression analysis indicated that the presence of Bartonella is more likely to occur in some flea species. From a subset of Bartonella-positive fleas, phylogenetic analyses of gltA gene sequences revealed 13 genetic variants clustering in five phylogroups (I­V), two of which were matched with known pathogenic Bartonella species (Bartonella vinsonii subsp. arupensis and Bartonella washoensis) and two that were not related with any previously described species or subspecies of Bartonella. Variants in phylogroup V, which were mainly obtained from Meringis spp. fleas, were identical to those reported recently in their specific rodent hosts (Dipodomys spp.) in the same region, suggesting that kangaroo rats and their fleas harbor other Bartonella species not reported previously. Considering the Bartonella prevalence and the flea genotypes associated with known pathogenic Bartonella species, we suggest that analysis of rodent and flea communities in the region should continue for their potential implications for human health. Given that nearby locations in the United States have reported Y. pestis in wild animals and their fleas, we suggest conducting larger-scale studies to increase our knowledge of this bacterium.

Prevalence and genetic diversity of Bartonella strains in rodents from northwestern Mexico.

Bartonella infections were investigated in wild rodents from northwestern Chihuahua, Mexico. A total of 489 rodents belonging to 14 species were surveyed in four areas. Bartonella bacteria were cultured from 50.1% of rodent samples (245/489). Infection rates ranged from 0% to 83.3% per rodent species, with no significant difference between sites except for Cynomys ludovicianus. Phylogenetic analyses of the citrate synthase gene (gltA) of the Bartonella isolates revealed 23 genetic variants (15 novel and 8 previously described), clustering into five phylogroups. Three phylogroups were associated with Bartonella vinsonii subsp. vinsonii, B. vinsonii subsp. arupensis, and B. washoensis, respectively. The other two phylogroups were not genetically related to any known Bartonella species. The genetic variants and phylogenetic groups exhibited a high degree of host specificity, mainly at the genus and family levels. This is the first study that describes the genetic diversity of Bartonella strains in wild rodents from Mexico. Considering that some variants found in this study are associated with Bartonella species that have been reported as zoonotic, more investigations are needed to further understand the ecology of Bartonella species in Mexican wildlife and their implications for human health.

Hematology and serum biochemistry values of Culpeo foxes (Lycalopex culpaeus) from central Chile.

Hematology and serum biochemistry values were determined for 31 healthy captive and free-ranging Culpeo foxes (Lycalopex culpaeus) sampled in central Chile between 2008 and 2012. The influences of sex, age, and origin (captive versus free-ranging foxes) on the blood parameters were evaluated. The blood values determined were generally comparable to commonly reported values for other wild canid species and the domestic dog. No differences attributable to sex were observed for any parameter. Juveniles had higher levels of alkaline phosphatase and phosphorus and lower values of mean corpuscular hemoglobin concentration, blood urea nitrogen, total protein, and globulin than adult foxes. Captive and free-ranging animals differed in glucose and albumin values. This is the first study on blood parameters of the Culpeo fox and represents a contribution for clinical evaluations of this carnivore in captivity as well as in the wild.

Responses of small mammals to habitat fragmentation: epidemiological considerations for rodent-borne hantaviruses in the Americas.

Rodent-borne hantaviruses are a group of zoonotic agents that cause hemorrhagic fever in humans. The transmission of hantaviruses among rodent hosts may be higher with the increase of reservoir host abundance in a given area (density-dependent transmission) and with the decrease of small mammal diversity (dilution effect phenomenon). These population and community parameters may be modified by habitat fragmentation; however, studies that focus on fragmentation and its effect on hantavirus infection risk are scarce. To further understanding of this issue, we assessed some population and community responses of rodents that may increase the risk for hantavirus transmission among wildlife hosts in the Americas. We conducted a meta-analysis of published studies to assess the responses of small mammals to fragmentation of native habitats, relative to patch size. Our analyses included five countries and 14 case studies for abundance of reservoir hosts (8 species) and 15 case studies for species richness. We found that a reduction of patch area due to habitat fragmentation is associated with increased reservoir host abundances and decreased small mammal richness, which is mainly due to the loss of non-host small mammals. According to these results, habitat fragmentation in the Americas should be considered as an epidemiological risk factor for hantavirus transmission to humans. These findings are important to assess potential risk of infection when fragmentation of native habitats occurs.

Ectoparasitism by Eutrombicula alfreddugesi larvae (Acari: Trombiculidae) on Liolaemus tenuis lizard in a Chilean fragmented temperate forest.

We compared parasite load (prevalence and mean intensity) of Eutrombicula alfreddugesi larvae on the lizard Liolaemus tenuis sampled during January 2006 and 2007 from the interior and edges of large forest tracts in the coastal Maulino Forest (35 degrees 59'S, 72 degrees 41'W) and from nearby forest fragments (1.5-20 ha). All lizards were parasitized by chiggers regardless of location (prevalence, 100%); however, mean intensity of infestation was significantly lower at forest fragment edges compared with either large forest interiors or forest edges. We attribute differences in mean intensity to differences in microclimate among localities; maximum air temperature was significantly higher and relative humidity significantly lower in fragment edges compared with either large forest tract interior or edges.