Leveraging location intelligence and individual-based modeling to simulate Rhipicephalus microplus infestation and eradication dynamics at the cattle-wildlife interface

Abstract

Cattle fever ticks (CFT), Rhipicephalus (Boophilus) annulatus and R. (B.) microplus, threaten the economic security of the USA cattle industry as vectors of Babesia bigemina and B. bovis. Of the two CFT, R. microplus has a more invasive biology and thrives in tropical and subtropical ecosystems. The U.S. Cattle Fever Tick Eradication Program successfully eliminated CFT from the southern USA and has since prevented CFT re-establishment by operating surveillance and quarantine in South Texas, including the permanent quarantine zone along the Texas-Mexico border. However, introductions and successful establishment of alternate CFT hosts, including white-tailed deer (Odocoileus virginianus) and nilgai (Boselaphus tragocamelus) in the Tamaulipan biome, have complicated eradication efforts. We used location intelligence and a spatially explicit, individual-based model to simulate potential impacts of wildlife hosts on R. microplus infestation/eradication dynamics in the Laguna Atascosa National Wildlife Refuge that encompasses a brushland ecosystem with diverse coastal habitats, including parts of a lagoon in South Texas. Results of our hypothetical eradication scenarios suggest that even sparse populations of wildlife hosts can maintain R. microplus populations in habitat-specific refugia during eradication efforts. The present model version is the first to have incorporated a georeferenced representation of a real landscape and to have integrated site-specific field data on climatic conditions and cattle movement patterns. Model forecasts of spatially explicit chronologies of changes in R. microplus densities can aid in a priori evaluation of field sampling strategies and treatment applications in specific landscapes under specific environmental conditions.

Keywords: Cattle fever tick; Individual-based model; Laguna Atascosa National Wildlife Refuge; Permanent quarantine zone; Spatially explicit model.

Graphical abstract

Fig. 1

A Map of the location of the study area (star) at the Laguna Atascosa National Wildlife Refuge (LANWR) in Cameron County, Texas, as well as the cattle fever tick permanent quarantine zone (purple). The study area was designated as an infested premise (red) by the Texas Animal Health Commission. Adjacent to these infested premises, a surveillance area (yellow) has been established. B Spatial distribution of the 11 vegetation types represented in the study area and in the model. Vegetation types include Loma Shrubland (green), Salty Prairie (yellow), Salt and Brackish High Tidal Shrub Wetland (brown), Loma Grassland (lime), Sea Ox-eye Daisy Flats (pink), Mangrove Shrubland (cyan), Salt and Brackish High Tidal Marsh (buff), Wind Tidal Flats (gray), Algal Flats (red), Barren (bright pink), and Open Water (blue).

Fig. 2

Conceptual model representing the potential role of white-tailed deer (Odocoileus virginianus) and nilgai (Boselaphus tragocamelus) in the maintenance of Rhipicephalus microplus populations in southern Texas and northeastern Mexico.

Fig. 3

Overview of the sequence of events and processes involved in the execution of the model.

Fig. 4

Spatial distribution of the 11 habitat types at the Laguna Atascosa National Wildlife Refuge (LANWR) in Cameron County, Texas grouped based on (A) their relative quality as survival habitat for off-host ticks (good, red; poor, orange; very poor, gray), (B) as foraging and browsing habitat for white-tailed deer and nilgai (good, red; fair, orange; poor, gray), and (C) as resting habitat for white-tailed deer and nilgai (good, red; fair, orange; poor, gray).

Fig. 5

A Total number of landscape cells infested during weeks 31 (2018) 52 (2019), with off-host larvae during simulations in which wildlife hosts were removed when acaricide-treated steers were introduced (Scenario 1, blue line) and during simulations in which wildlife hosts were not removed (Scenario 2, orange line). Also shown are numbers of cells characterized as good (B) and poor (C) tick habitats infested during simulations. (No very poor tick habitat cells were infested.) Gray vertical lines indicate the period during which steers were present. Good tick habitats include Loma Shrubland. Poor tick habitats include Salty Prairie, Salt and Brackish High Tidal Shrub Wetland, and Loma Grassland. Very poor tick habitats include Sea Ox-eye Daisy Flats, Mangrove Shrubland, Salt and Brackish High Tidal Marsh, Wind Tidal Flats, Algal Flats, Barren, and Open Water.

Fig. 6

The distribution of landscape cells infested during weeks 31 (2018) 52 (2019), with off-host larvae among cells characterized as good, poor, and very poor tick habitats (A) at the time the acaricide-treated steers were introduced and (B) at the time they were removed. Results are shown both for simulations in which wildlife hosts were removed when acaricide-treated steers were introduced (Scenario 1 - S1) and for simulations in which wildlife hosts were not removed (Scenario 2 - S2). See Fig. 5 for specific habitats included in good, poor, and very poor categories.

Fig. 7

A Total number of landscape cells infested during weeks 31 (2018) 52 (2019), with off-host larvae. B Number of cells characterized as good tick habitats infested during simulations in which steers were never introduced (Scenario 3). Gray vertical lines indicate the period during which steers were present in Scenarios 1 and 2. Also shown are the distributions of landscape cells infested with off-host larvae among cells characterized as good, poor, and very poor tick habitats (C) at the time the acaricide-treated steers were introduced in Scenarios 1 & 2 and (D) at the time they were removed in those scenarios. See Fig. 5 for specific habitats included in good, poor, and very poor categories.

Fig. 8

Spatial distributions of host-seeking larval ticks (red). Top maps indicate distributions at the time the acaricide-treated steers were introduced in simulations in which (A) wildlife hosts were removed (Scenario 1) and (B) wildlife hosts were not removed (Scenario 2). Bottom maps indicate distributions at the time the steers were removed in simulations of (C) Scenario 1 and (D) Scenario 2. The number of infested cells is given in parentheses. White dots represent the locations of wildlife hosts at the indicated times. See Fig. 1 for specific vegetation type and associated color description.

Fig. 9

Spatial distributions of host-seeking larval ticks (red) in simulations in which the steers were never present (Scenario 3): (A) at the time the acaricide-treated steers were introduced in Scenarios 1 & 2 (August 2019) and (B) at the time the steers were removed in Scenarios 1 & 2 (mid-December 2019). The number of infested cells is given in parentheses. White dots represent the locations of wildlife hosts at the indicated times. See Fig. 1 for specific vegetation type and associated color description.

Fig. 10

Percentage of time spent by white-tailed deer (blue bars), nilgai (orange bars), and acaricide-treated steers (gray bars) in each of the 11 vegetation types (A) and in good, poor, and very poor tick habitats (B). Vegetation types include Salty Prairie (#1), Sea Ox-eye Daisy Flats (#2), Mangrove Shrubland (#3), Salt and Brackish High Tidal Shrub Wetland (#4), Salt and Brackish High Tidal Marsh (#5), Wind Tidal Flats (#6), Algal Flats (#7), Loma Shrubland (#8), Loma Grassland (#9), Barren (#10), and Open Water (#11).

Fig. 11

Total number of landscape cells infested during weeks 31 (2018) to 52 (2019), with off-host larvae (A) and number of cells characterized as good tick habitat infested during simulations in which host densities were reduced (B). Dark blue, orange, green, yellow, and light blue represent simulations in which host densities were reduced to 1/2, 1/4, 1/8, 1/16, and 1/32 of their baseline densities. Gray vertical lines indicate the period during which the acaricide-treated steers were present. Also shown are the number of landscape cells infested during simulations at the indicated host densities (C) at the time the steers were introduced and at the time they were removed (D). Sets of bars represent distributions of landscape cells infested with off-host larvae among cells characterized as good, poor, and very poor tick habitats. See Fig. 5 for specific habitats included in good, poor, and very poor categories.

Fig. 12

Spatial distributions of host-seeking larval ticks (red). Top maps indicate distributions at the time the acaricide-treated steers were introduced in simulations in which wildlife host densities were reduced to 1/2 of their baseline densities (Scenario 4a) (A) and wildlife host densities were reduced to 1/32 of their baseline densities (Scenario 4e) (B). Bottom maps indicate distributions at the time the steers were removed in simulations of Scenario 4a (C) and Scenario 4e (D). The number of infested cells is given in parentheses. White dots represent the locations of wildlife hosts at the indicated times. See Fig. 1 for specific vegetation type and associated color description.

Fig. 13

Number of larvae-infested landscape cells in each of the three most infested habitat types at the time the steers were introduced (A) and at the time they were removed (B). Bars on the left are results from simulations in which wildlife host densities were reduced to 1/2 of their baseline densities (Scenario 4a). Bars on the right are results from simulations in which wildlife host densities were reduced to 1/32 of their baseline densities (Scenario 4e). The vegetation types are Salty Prairie (#1), Loma Shrubland (#8), and Loma Grassland (#9).