Ticks (Acari: Ixodida) on synanthropic small and medium-sized mammals in areas of the northeastern United States infested with the Asian longhorned tick, Haemaphysalis longicornis.

The northeastern United States (US) is a hotspot for tick-borne diseases. Adding to an already complex vector landscape, in 2017 large populations of the invasive Haemaphysalis longicornis, the Asian longhorned tick, were detected in New Jersey (NJ) and later found to be widespread from Connecticut to Georgia. In its native range in northeastern Asia, H. longicornis is considered an important vector of deadly pathogens to humans, companion animals, and livestock. To identify the primary hosts of H. longicornis, we surveyed synanthropic small and medium-sized mammals in three different sites in suburban New Brunswick, NJ. Specifically, we collected approximately 9,000 tick specimens belonging to nine species from 11 different species of mammals sampled between May and September 2021. We found that H. longicornis feeds more frequently on rodents than previously thought, and that this invasive tick is likely exposed to important enzootic and zoonotic pathogens. Overall, we obtained detailed information about the seasonal dynamics and feeding patterns of six tick species common in the northeastern US, Haemaphysalis longicornis, Amblyomma americanum, Dermacentor variabilis, Ixodes scapularis, Ixodes texanus and Ixodes cookei. We found that unlike I. scapularis that feeds on mammals of all sizes, H. longicornis feeds on hosts following the general pattern of A. americanum, favoring larger species such as skunks, groundhogs, and raccoons. However, our survey revealed that unlike A. americanum, H. longicornis reaches high densities on Virginia opossum. Overall, the newly invasive H. longicornis was the most numerous tick species, both on multiple host species and in the environment, raising significant questions regarding its role in the epidemiology of tick-borne pathogens, especially those affecting livestock, companion animals and wildlife. In conclusion, our findings provide valuable insights into the tick species composition on mammalian hosts in NJ and the ongoing national expansion of H. longicornis.

Pathogen Coinfections Harbored by Adult Ixodes scapularis from White-Tailed Deer Compared with Questing Adults Across Sites in Maryland, USA.

The blacklegged tick, Ixodes scapularis, can acquire and transmit tick-borne pathogens (TBPs) responsible for diseases such as human granulocytic anaplasmosis (Anaplasma phagocytophilum [ANPH]), babesiosis (Babesia microti [BABE]), Lyme borreliosis (Borrelia burgdorferi sensu lato [BBSL]), and the relatively novel relapsing fever-like illness, Borrelia miyamotoi (BMIY) disease in the northeastern United States. Coinfections with these pathogens are becoming increasingly more common in I. scapularis and their hosts, likely attributed to their shared enzootic cycles. Urban habitats are favorable to host species such as white-tailed deer (Odocoileus virginianus) and these ungulates are known to be important to I. scapularis for reproduction and dispersal in North America. To understand the relationship between TBPs, white-tailed deer, and I. scapularis, we sampled eight sites across central Maryland collecting I. scapularis using standard tick dragging/flagging methods and retrieved others from deer carcasses. Pathogenic TBP species in each tick were determined using qPCR. In total, 903 adult ticks (deer: n = 573; questing: n = 330) revealed landscape-level prevalence of ANPH (27.8%), BABE (1.3%), BBSL (14.6%), and BMIY (0.8%) as singular infections overall. However, secondary coinfections of ANPH and BBSL were highest (9.9%) in ticks feeding from deer while associations of BBSL and BABE (4.2%) were highest in questing ticks. Results from this study provide evidence suggesting that adult I. scapularis acquire pathogenic species through phenologically associated host use, and thus, subsequent infections found in adults may provide insights into coinfection relationships.

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'.

Surveillance of Ticks and Tick-Borne Pathogens in Suburban Natural Habitats of Central Maryland.

Lyme and other tick-borne diseases are increasing in the eastern United States and there is a lack of research on integrated strategies to control tick vectors. Here we present results of a study on tick-borne pathogens detected from tick vectors and rodent reservoirs from an ongoing 5-yr tick suppression study in the Lyme disease-endemic state of Maryland, where human-biting tick species, including Ixodes scapularis Say (Acari: Ixodidae) (the primary vector of Lyme disease spirochetes), are abundant. During the 2017 tick season, we collected 207 questing ticks and 602 ticks recovered from 327 mice (Peromyscus spp. (Rodentia: Cricetidae)), together with blood and ear tissue from the mice, at seven suburban parks in Howard County. Ticks were selectively tested for the presence of the causative agents of Lyme disease (Borrelia burgdorferi sensu lato [s.l.]), anaplasmosis (Anaplasma phagocytophilum), babesiosis (Babesia microti), ehrlichiosis (Ehrlichia ewingii, Ehrlichia chaffeensis, and 'Panola Mountain' Ehrlichia) and spotted fever group rickettsiosis (Rickettsia spp.). Peromyscus ear tissue and blood samples were tested for Bo. burgdorferi sensu stricto (s.s), A. phagocytophilum, Ba. microti, and Borrelia miyamotoi. We found 13.6% (15/110) of questing I. scapularis nymphs to be Bo. burgdorferi s.l. positive and 1.8% (2/110) were A. phagocytophilum positive among all sites. Borrelia burgdorferi s.s. was found in 71.1% (54/76) of I. scapularis nymphs removed from mice and 58.8% (194/330) of captured mice. Results from study on tick abundance and pathogen infection status in questing ticks, rodent reservoirs, and ticks feeding on Peromyscus spp. will aid efficacy evaluation of the integrated tick management measures being implemented.

Prevalence of protozoan parasites in small and medium mammals in Texas, USA.

Wildlife interaction with humans increases the risk of potentially infected ticks seeking an opportunistic blood meal and consequently leading to zoonotic transmission. In the United States, human babesiosis is a tick-borne zoonosis most commonly caused by the intraerythrocytic protozoan parasite, Babesia microti. The presence of Babesia microti and other species of Babesia within Texas has not been well characterized, and the molecular prevalence of these pathogens within wildlife species is largely unknown. Small (e.g. rodents) and medium sized mammalian species (e.g. racoons) represent potential reservoirs for specific species of Babesia, though this relationship has not been thoroughly evaluated within Texas. This study aimed to characterize the molecular prevalence of Babesia species within small and medium sized mammals at two sites in East Texas with an emphasis on detection of pathogen presence in these two contrasting wild mammal groups at these sites. To that end, a total of 480 wild mammals representing eight genera were trapped, sampled, and screened for Babesia species using the TickPath layerplex qPCR assay. Two sites were selected for animal collection, including The Big Thicket National Preserve and Gus Engeling Wildlife Management Area. Molecular analysis revealed the prevalence of various Babesia and Hepathozoon species at 0.09% each, and Sarcocystis at 0.06% . Continued molecular prevalence surveys of tick-borne pathogens in Texas wild mammals will be needed to provide novel information as to which species of Babesia are most prevalent and identify specific wildlife species as pathogen reservoirs.

The Ecology and Phylogeny of Hosts Drive the Enzootic Infection Cycles of Hantaviruses.

Hantaviruses (Family: Hantaviridae; genus: Orthohantavirus) and their associated human diseases occur globally and differ according to their geographic distribution. The structure of small mammal assemblages and phylogenetic relatedness among host species are suggested as strong drivers for the maintenance and spread of hantavirus infections in small mammals. We developed predictive models for hantavirus infection prevalence in rodent assemblages using defined ecological correlates from our current knowledge of hantavirus-host distributions to provide predictive models at the global and continental scale. We utilized data from published research between 1971-2014 and determined the biological and ecological characteristics of small mammal assemblages to predict the prevalence of hantavirus infections. These models are useful in predicting hantavirus disease outbreaks based on environmental and biological information obtained through the surveillance of rodents.

Detection of New World Hantavirus Antibodies in Rodents of Eastern New Mexico, USA.

Hantaviruses, causal agents of the potentially lethal hantavirus pulmonary syndrome, have widely distributed rodent hosts. Using an enzyme-linked immunosorbent assay, we tested blood from 398 wild rodents captured in eastern New Mexico, US in 2015-17 and found 42 antibody-positive samples representing six genera.

Global Diversity and Distribution of Hantaviruses and Their Hosts.

Rodents represent 42% of the world's mammalian biodiversity encompassing 2,277 species populating every continent (except Antarctica) and are reservoir hosts for a wide diversity of disease agents. Thus, knowing the identity, diversity, host-pathogen relationships, and geographic distribution of rodent-borne zoonotic pathogens, is essential for predicting and mitigating zoonotic disease outbreaks. Hantaviruses are hosted by numerous rodent reservoirs. However, the diversity of rodents harboring hantaviruses is likely unknown because research is biased toward specific reservoir hosts and viruses. An up-to-date, systematic review covering all known rodent hosts is lacking. Herein, we document gaps in our knowledge of the diversity and distribution of rodent species that host hantaviruses. Of the currently recognized 681 cricetid, 730 murid, 61 nesomyid, and 278 sciurid species, we determined that 11.3, 2.1, 1.6, and 1.1%, respectively, have known associations with hantaviruses. The diversity of hantaviruses hosted by rodents and their distribution among host species supports a reassessment of the paradigm that each virus is associated with a single-host species. We examine these host-virus associations on a global taxonomic and geographical scale with emphasis on the rodent host diversity and distribution. Previous reviews have been centered on the viruses and not the mammalian hosts. Thus, we provide a perspective not previously addressed.

The Prevalence of Trypanosoma cruzi, the Causal Agent of Chagas Disease, in Texas Rodent Populations.

Rodent species were assessed as potential hosts of Trypanosoma cruzi, the etiologic agent of Chagas disease, from five sites throughout Texas in sylvan and disturbed habitats. A total of 592 rodents were captured, resulting in a wide taxonomic representation of 11 genera and 15 species. Heart samples of 543 individuals were successfully analyzed by SybrGreen-based quantitative PCR (qPCR) targeting a 166 bp fragment of satellite DNA of T. cruzi. Eight rodents representing six species from six genera and two families were infected with T. cruzi. This is the first report of T. cruzi in the pygmy mouse (Baiomys taylori) and the white-footed mouse (Peromyscus leucopus) for the USA. All infected rodents were from the southernmost site (Las Palomas Wildlife Management Area). No differences in pathogen prevalence existed between disturbed habitats (5 of 131 tested; 3.8%) and sylvan habitats (3 of 40 tested; 7.5%). Most positives (n = 6, 16% prevalence) were detected in late winter with single positives in both spring (3% prevalence) and fall (1% prevalence). Additionally, 30 Triatoma insects were collected opportunistically from sites in central Texas. Fifty percent of these insects, i.e., 13 T. gerstaeckeri (68%), and two T. lecticularia (100%) were positive for T. cruzi. Comparative sequence analyses of 18S rRNA of samples provided identical results with respect to detection of the presence or absence of T. cruzi and assigned T. cruzi from rodents collected in late winter to lineage TcI. T. cruzi from Triatoma sp. and rodents from subsequent collections in spring and fall were different, however, and could not be assigned to other lineages with certainty.

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.