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      Enhanced biosurveillance of high-consequence invasive pests: southern cattle fever ticks, Rhipicephalus ( Boophilus) microplus, on livestock and wildlife

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          Abstract

          Background

          Some tick species are invasive and of high consequence to public and veterinary health. Socioeconomic development of rural parts of the USA was enabled partly through the eradication by 1943 of cattle fever ticks (CFT, Rhipicephalus ( Boophilus) annulatus and R. ( B.) microplus). The southern cattle fever ticks (SCFT, R. ( B.) microplus) remain a real and present threat to the USA animal agriculture because they are established in Mexico. Livestock-wildlife interactions in the Permanent Quarantine Zone (PQZ) established by the century-old Cattle Fever Tick Eradication Programme (CFTEP) in south Texas endanger its operations.

          Methods

          We describe a spatially-explicit, individual-based model that simulates interactions between cattle, white-tailed deer (WTD, Odocoileus virginianus), and nilgai ( Boselaphus tragocamelus) to assess the risk for SCFT infestations across the pathogenic landscape in the PQZ and beyond. We also investigate the potential role of nilgai in sustaining SCFT populations by simulating various hypothetical infestation and eradication scenarios.

          Results

          All infestation scenarios resulted in a phase transition from a relatively small proportion of the ranch infested to almost the entire ranch infested coinciding with the typical period of autumn increases in off-host tick larvae. Results of eradication scenarios suggest that elimination of all on-host ticks on cattle, WTD, or nilgai would have virtually no effect on the proportion of the ranch infested or on the proportions of different tick habitat types infested; the entire ranch would remain infested. If all on-host ticks were eliminated on cattle and WTD, WTD and nilgai, or cattle and nilgai, the proportions of the ranch infested occasionally would drop to 0.6, 0.6 and 0.2, respectively. Differences in proportions of the ranch infested from year to year were due to primarily to differences in winter weather conditions, whereas infestation differences among tick habitat types were due primarily to habitat use preferences of hosts.

          Conclusions

          Infestations in nilgai augment SCFT refugia enabled by WTD and promote pest persistence across the landscape and cattle parasitism. Our study documented the utility of enhanced biosurveillance using simulation tools to mitigate risk and enhance operations of area-wide tick management programmes like the CFTEP through integrated tactics for SCFT suppression.

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          Most cited references34

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          A review of bovine anaplasmosis.

          Bovine anaplasmosis, caused by Anaplasma marginale, is an infectious but non-contagious disease. It is spread through tick bites or by the mechanical transfer of fresh blood from infected to susceptible cattle from biting flies or by blood-contaminated fomites including needles, ear tagging, dehorning and castration equipment. Transplacental transmission of A. marginale may contribute to the epidemiology of bovine anaplasmosis in some regions. Bovine anaplasmosis occurs in tropical and subtropical regions worldwide. Cattle of all ages are susceptible to infection with A. marginale, but the severity of disease increases with age. Once cattle of any age become infected with A. marginale, they remain persistently infected carriers for life. Diagnosis of bovine anaplasmosis can be made by demonstration of A. marginale on stained blood smears from clinically infected animals during the acute phase of the disease, but it is not reliable for detecting infection in pre-symptomatic or carrier animals. In these instances, the infection is generally diagnosed by serologic demonstration of antibodies with confirmation by molecular detection methods. The susceptibility of wild ruminants to infection by A. marginale and the role of wild ruminants in the epidemiology of bovine anaplasmosis are incompletely known owing to lack of published research, lack of validation of diagnostic tests for these species and cross-reaction of Anaplasma spp. antibodies in serologic tests. Control measures for bovine anaplasmosis vary with geographical location and include maintenance of Anaplasma-free herds, vector control, administration of antibiotics and vaccination. © 2010 Crown in the right of Canada.
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            Climate, niche, ticks, and models: what they are and how we should interpret them.

            Ticks spend most of their life cycle in the environment, and all tick life cycle stages are dependent on a complex combination of climate variables. Furthermore, host availability and vegetation significantly modulate the dynamics of tick populations. Tick recruitment is dependent on successful reproduction, which in turn requires sufficient adult tick densities, available blood meal sources, and egg survival. Though many animals can serve as hosts, there are several determinants of host suitability. For example, host availability in time and space is an important determinant of tick bionomics. Shelter and protection from environmental extremes are critical to tick survival. Questing and diapausing ticks are vulnerable to extremes of temperature and humidity. There are concerns about how predicted climate change may alter several critical features of host-parasite relationships of ticks, the potential for invasion of new areas or alteration of patterns of pathogen transmission in particular. However, modeling approaches that relate known occurrences of tick species to climate (and/or landscape) features and predict geographic occurrences are not completely fulfilling our needs to understand how the "tick panorama" can change as a consequence of these climate trends. This is a short review about the concept of ecological niche as applied to ticks, as well as some raised concerns about its evaluation and strict definition, and its usefulness to map geographical suitability for ticks. Comments about how climate, hosts, and landscape configuration are briefly discussed regarding its applicability to tick mapping and with reference about their impact on tick abundance. I will further comment on already published observations about observed changes in the geographical range of ticks in parts of Europe.
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              Widespread movement of invasive cattle fever ticks (Rhipicephalus microplus) in southern Texas leads to shared local infestations on cattle and deer

              Background Rhipicephalus (Boophilus) microplus is a highly-invasive tick that transmits the cattle parasites (Babesia bovis and B. bigemina) that cause cattle fever. R. microplus and Babesia are endemic in Mexico and ticks persist in the United States inside a narrow tick eradication quarantine area (TEQA) along the Rio Grande. This containment area is threatened by unregulated movements of illegal cattle and wildlife like white-tailed deer (WTD; Odocoileus virginianus). Methods Using 11 microsatellite loci we genotyped 1,247 R. microplus from 63 Texas collections, including outbreak infestations from outside the TEQA. We used population genetic analyses to test hypotheses about ecological persistence, tick movement, and impacts of the eradication program in southern Texas. We tested acaricide resistance with larval packet tests (LPTs) on 47 collections. Results LPTs revealed acaricide resistance in 15/47 collections (32%); 11 were outside the TEQA and three were resistant to multiple acaricides. Some collections highly resistant to permethrin were found on cattle and WTD. Analysis of genetic differentiation over time at seven properties revealed local gene pools with very low levels of differentiation (F ST 0.00-0.05), indicating persistence over timespans of up to 29 months. However, in one neighborhood differentiation varied greatly over a 12-month period (F ST 0.03-0.13), suggesting recurring immigration from distinct sources as another persistence mechanism. Ticks collected from cattle and WTD at the same location are not differentiated (F ST = 0), implicating ticks from WTD as a source of ticks on cattle (and vice versa) and emphasizing the importance of WTD to tick control strategies. We identified four major genetic groups (K = 4) using Bayesian population assignment, suggesting multiple introductions to Texas. Conclusions Two dispersal mechanisms give rise to new tick infestations: 1) frequent short-distance dispersal from the TEQA; and 2) rare long-distance, human-mediated dispersal from populations outside our study area, probably Mexico. The threat of cattle fever tick transport into Texas is increased by acaricide resistance and the ability of R. microplus to utilize WTD as an alternate host. Population genetic analyses may provide a powerful tool for tracking invasions in other parts of the world where these ticks are established.
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                Author and article information

                Contributors
                hsuan006@tamu.edu
                wegrant@tamu.edu
                pteel@tamu.edu
                kim.lohmeyer@usda.gov
                beto.perezdeleon@usda.gov
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                23 September 2020
                23 September 2020
                2020
                : 13
                : 487
                Affiliations
                [1 ]GRID grid.264756.4, ISNI 0000 0004 4687 2082, Ecological Systems Laboratory, Department of Ecology and Conservation Biology, , Texas A&M University, ; College Station, TX 77843 USA
                [2 ]GRID grid.264756.4, ISNI 0000 0004 4687 2082, Department of Entomology, , Texas A&M AgriLife Research, ; College Station, TX 77843 USA
                [3 ]GRID grid.463419.d, ISNI 0000 0001 0946 3608, United States Department of Agriculture – Agricultural Research Service, , Knipling-Bushland U.S. Livestock Insects Research Laboratory, and Veterinary Pest Genomics Center, ; Kerrville, TX 78028 USA
                Author information
                http://orcid.org/0000-0002-7850-0406
                Article
                4366
                10.1186/s13071-020-04366-x
                7513513
                90edfcbf-166e-4e74-9586-635fce83339d
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 22 January 2020
                : 17 September 2020
                Funding
                Funded by: USDA-ARS
                Award ID: 3094-32000-039-93S
                Award ID: 3094-32000-039-00-D
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Parasitology
                cattle fever tick eradication program,host-parasite interaction,individual-based model,spatially-explicit model,stochastic,integrated tick management research,rhipicephalus microplus

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