A.A. Pérez de León

Facilitative Ecological Interactions between Invasive Species: Arundo donax Stands as Favorable Habitat for Cattle Ticks (Acari: Ixodidae) Along the U.S.-Mexico Border

ABSTRACT The cattle tick, Rhipicephalus (Boophilus) spp. is a key vector of protozoa that cause bovine babesiosis. Largely eradicated from most of the United States, the cattle tick continues to infest south Texas, and recent outbreaks in this area may signal a resurgence of cattle tick populations despite current management efforts. An improved understanding of the dynamic ecology of cattle fever ticks along the U.S.-Mexico border is required to devise strategies for sustainable eradication efforts. Management areas of the cattle tick overlap considerably with dense, wide infestations of the non-native, invasive grass known as giant reed (Arundo donax L.). Here we show that stands of giant reed are associated with abiotic and biotic conditions that are favorable to tick survival, especially when compared with other nearby habitats (open pastures of buffelgrass (Pennisetum ciliare) and closed canopy native forests). Overhead canopies in giant reed stands and native riparian forests reduce daily high temperature, which was the best abiotic predictor of oviposition by engorged females. In sites where temperatures were extreme, specifically open grasslands, fewer females laid eggs and the resulting egg masses were smaller. Pitfall trap collections of ground dwelling arthropods suggest a low potential for natural suppression of tick populations in giant reed stands. The finding that A. donax infestations present environmental conditions that facilitate the survival and persistence of cattle ticks, as well or better than native riparian habitats and open grasslands, represents an alarming complication for cattle fever tick management in the United States.

Ticks collected from humans, domestic animals, and wildlife in Yucatan, Mexico.

Domestic animals and wildlife play important roles as reservoirs of zoonotic pathogens that are transmitted to humans by ticks. Besides their role as vectors of several classes of microorganisms of veterinary and public health relevance, ticks also burden human and animal populations through their obligate blood-feeding habit. It is estimated that in Mexico there are around 100 tick species belonging to the Ixodidae and Argasidae families. Information is lacking on tick species that affect humans, domestic animals, and wildlife through their life cycle. This study was conducted to bridge that knowledge gap by inventorying tick species that infest humans, domestic animals and wildlife in the State of Yucatan, Mexico. Amblyomma ticks were observed as euryxenous vertebrate parasites because they were found parasitizing 17 animal species and human. Amblyomma mixtum was the most eryxenous species found in 11 different animal species and humans. Both A. mixtum and A. parvum were found parasitizing humans. Ixodes near affinis was the second most abundant species parasitizing six animal species (dogs, cats, horses, white-nosed coati, white-tail deer and black vulture) and was found widely across the State of Yucatan. Ixodid tick populations may increase in the State of Yucatan with time due to animal production intensification, an increasing wildlife population near rural communities because of natural habitat reduction and fragmentation. The diversity of ticks across host taxa documented here highlights the relevance of ecological information to understand tick-host dynamics. This knowledge is critical to inform public health and veterinary programs for the sustainable control of ticks and tick-borne diseases.

Acaricide and ivermectin resistance in a field population of Rhipicephalus microplus (Acari: Ixodidae) collected from red deer (Cervus elaphus) in the Mexican tropics

In the Neotropics the control of tick infestations in red deer (Cervus elaphus) is achieved primarily through the use of acaricides and macrocyclic lactones. In Mexico, resistance to one or multiple classes of acaricides has been reported in Rhipicephalus microplus infesting cattle, but information on acaricide susceptibility in R. microplus infesting red deer is lacking. In this study we report the level of resistance to different classes of acaricides and ivermectin in R. microplus collected from red deer in the Mexican tropics. Engorged R. microplus females were collected from a red deer farm in Yucatan, Mexico. The larval packet test was used to detect resistance to the organophosphates (OPs) chlorpyrifos and coumaphos, synthetic pyrethroids (SPs) cypermethrin and permethrin, and the phenylpyrazol, fipronil. Resistance to the formamidine amitraz (Am), and ivermectin was ascertained using the larval immersion test. Data were subjected to probit analysis to determine lethal concentrations and resistance ratios to kill 50% (RR50) and 99% (RR99) of the tick population under evaluation in relation to susceptible reference strains. Additionally, allele specific polymerase chain reaction was used to detect the sodium channel F1550I mutation associated with SP resistance in R. microplus. The R. microplus population from red deer in Yucatan showed very high resistance to the two SPs evaluated (RRs>72.2 for cypermethrin; RR for permethrin resistance was so high a dose-response curve was not possible). All individual larvae tested to detect the sodium channel F1550I mutation associated with SP resistance in R. microplus were homozygous. The same tick population showed different levels of resistance to OPs (chlorpyrifos: RR50=1.55, RR99=0.63; coumaphos: RR50=6.8, RR99=5.9), fipronil (RR50=1.8, RR99=0.9), and amitraz (RR50=2.3, RR99=4.4). Resistance to ivermectin was regarded as moderate (RR50=7.1, RR99=5.0). This is the first report of R. microplus ticks collected from red deer in Mexico with different levels of resistance to four acaricide groups and ivermectin.

In vitro and in vivo evaluation of cypermethrin, amitraz, and piperonyl butoxide mixtures for the control of resistant Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in the Mexican tropics

A study was conducted to evaluate the efficacy of cypermethrin, amitraz, and piperonyl butoxide (PBO) mixtures, through in vitro laboratory bioassays and in vivo on-animal efficacy trials, for the control of resistant Rhipicephalus (Boophilus) microplus on cattle in the Mexican tropics. Also, to examine mechanisms of resistance to cypermethrin in this tick population, the frequency of a mutated sodium channel gene (F1550I) was determined using a PCR assay. Results of laboratory bioassays using modified larval packet tests revealed that cypermethrin toxicity was synergized by PBO (from 46.6-57.0% to 83.7-85.0% larval mortality; P<0.05). The cypermethrin and amitraz mixture showed an additive effect (from 46.6-57.0% to 56.0-74.3% larval mortality). Strong synergism was observed with the mixture of cypermethrin+amitraz+PBO and this mixture was the most effective killing resistant tick larvae in vitro (96.7-100% of larval mortality). Tick larvae surviving exposure to cypermethrin or mixtures either with amitraz and PBO in vitro showed 2.9-49.6 higher probability to present the mutated allele than those killed by acaricide treatment (P<0.05). In the in vivo trial, the mixtures containing cypermethrin+PBO (80.6-97.3%), and cypermethrin+amitraz (87.0-89.7%) were more efficacious than cypermethrin alone (76.3-80.5%). The highest level of efficacy was obtained with the mixture of cypermethrin+amitraz+PBO, which yielded >95% control that persisted for 28 days post-treatment against R. microplus infesting cattle when tested under field conditions in the Mexican tropics. Although this mixture is a potentially useful tool to combat pyrethroid resistance, a product based on an acaricide mixture like the one tested in this study has to be used rationally.

Effects of pyriproxyfen and buprofezin on immature development and reproduction in the stable fly

The stable fly, Stomoxys calcitrans (L.) (Diptera: Muscidae), is one of the most significant biting flies that affect cattle. The use of traditional insecticides for stable fly control has only a limited success owing to the insects unique feeding behaviours and immature development sites. A laboratory study was conducted to evaluate the effects of two insect growth regulator (IGR) products, pyriproxyfen and buprofezin, on the development of the immature stages of the stable fly and the effects of pyriproxyfen on oviposition and egg hatch. Both pyriproxyfen and buprofezin had significant inhibitory effects on immature development. The LC50s of pyriproxyfen and buprofezin were 0.002 and 18.92 p.p.m., respectively. Topical treatment of adult females with different doses of pyriproxyfen had significant negative effects on both female oviposition and egg hatching when 1‐ and 3‐day‐old females were treated, and the effects were dose dependent. A significant reduction in the mean number of eggs laid was observed only at the highest pyriproxyfen dose (8 µg/fly) and egg hatch was unaffected by pyriproxyfen treatment when 5‐day‐old females were treated. Results from the present study indicate that pyriproxyfen has the potential to be used as part of an integrated stable fly management programme.

First documentation of ivermectin resistance in Rhipicephalus sanguineus sensu lato (Acari: Ixodidae)

The brown dog tick, Rhipicephalus sanguineus sensu lato (Latreille, 1806), is an ectoparasite and disease vector of significant veterinary and public health importance that is distributed widely around the world. The intensive use of synthetic acaricides for tick control exerts a strong selective pressure for brown dog ticks to become resistant to them. Here, we investigated claims from the field regarding treatment failure associated with the use of veterinary products containing ivermectin (IVM) to control brown dog ticks infesting dogs in Yucatan state, Mexico. Dogs in six state municipalities were inspected to sample 15 R. sanguineus s.l. POPULATIONS Interviews were conducted with dog owners to gather information on the history of dog treatment with conventional acaricides and IVM. The larval immersion test was used on the progeny of adult female ticks infesting dogs to test for susceptibility to IVM. Dose-mortality regressions, lethal concentrations (LC), their confidence intervals, and slope were estimated by probit analysis. Ten tick populations (66.7%) were classified as resistant compared with the most susceptible population. A high inter-population variation in the phenotypic level of IVM resistance was evident (resistance ratio at LC50% and LC99% ranged from 1.0 to 30.5, and from 1.0 to 458.8, respectively). Tick populations classified as resistant were collected from dogs known to have been treated with IVM. To our knowledge, this is the first report of IVM resistance in R. sanguineus s.l. worldwide. Veterinary and pet owner education on integrated tick management practices is required to avoid widespread resistance and increased treatment failure with products containing IVM and other macrocyclic lactones used to control endo- and ectoparasites affecting dogs. Integrated tick management will also help mitigate the burden of brown dog tick-borne diseases on human and animal populations.

Spatial multi-criteria decision analysis for modelling suitable habitats of Ornithodoros soft ticks in the Western Palearctic region

Ticks are economically and medically important ectoparasites due to the injuries inflicted through their bite, and their ability to transmit pathogens to humans, livestock, and wildlife. Whereas hard ticks have been intensively studied, little is known about soft ticks, even though they can also transmit pathogens, including African Swine Fever Virus (ASFV) affecting domestic and wild suids or Borrelia bacteria causing tick-borne relapsing fever (TBRF) in humans. We thus developed a regional model to identify suitable spatial areas for a community of nine Ornithodoros tick species (O. erraticus, O. sonrai, O. alactagalis, O. nereensis, O. tholozani, O. papillipes, O. tartakovskyi, O. asperus, O. verrucosus), which may be of medical and veterinary importance in the Western Palearctic region. Multi-Criteria Decision Analysis was used due to the relative scarcity of high-quality occurrence data. After an in-depth literature review on the ecological requirements of the selected tick community, five climate-related factors appeared critical for feeding activity and tick development: (i) a spring temperature exceeding 10°C to induce the end of winter soft tick quiescent period, (ii) a three-months summer temperature above 20°C to allow tick physiological activities, (iii) annual precipitation ranging from 60mm to 750mm and, in very arid areas, (iv) dry seasons interrupted by small rain showers to maintain minimum moisture inside their habitat along the year or (v) residual water provided by perennial rivers near habitats. We deliberately chose not to include biological factors such as host availability or vegetation patterns. A sensitivity analysis was done by performing multiple runs of the model altering the environmental variables, their suitability function, and their attributed weights. To validate the models, we used 355 occurrence data points, complemented by random points within sampled ecoregions. All models indicated suitable areas in the Mediterranean Basin and semi-desert areas in South-West and Central Asia. Most variability between models was observed along northern and southern edges of highly suitable areas. The predictions featured a relatively good accuracy with an average Area Under Curve (AUC) of 0.779. These first models provide a useful tool for estimating the global distribution of Ornithodoros ticks and targeting their surveillance in the Western Palearctic region.

Introducción, Establecimiento, y Dispersión en México de la Avispa Tetramesa romana 1 , Agente de Control Biológico del Carrizo Gigante

Resumen. Arundo donax (carrizo gigante) es una especie exótica invasora que afecta la disponibilidad del agua. Esta planta fue declarada como especie nociva tanto en los Estados Unidos como en México. Para su control se estableció un programa de colaboración entre los Estados Unidos y México. Contando con la autorización correspondiente, la avispa Tetramesa romana fue liberada en 6 sitios en Morelos y 3 en Nuevo Laredo, Tamaulipas. Tetramesa romana se estableció en todos los sitios de liberación y sus efectos sobre el control de A. donax están siendo evaluados.

Movement patterns of nilgai antelope in South Texas: Implications for cattle fever tick management

Wildlife, both native and introduced, can harbor and spread diseases of importance to the livestock industry. Describing movement patterns of such wildlife is essential to formulate effective disease management strategies. Nilgai antelope (Boselaphus tragocamelus) are a free-ranging, introduced ungulate in southern Texas known to carry cattle fever ticks (CFT, Rhipicephalus (Boophilus) microplus, R. (B.) annulatus). CFT are the vector for the etiological agent of bovine babesiosis, a lethal disease causing high mortality in susceptible Bos taurus populations and severely affecting the beef cattle industry. Efforts to eradicate CFT from the United States have been successful. However, a permanent quarantine area is maintained between Texas and Mexico to check its entry from infested areas of neighboring Mexico states on wildlife and stray cattle. In recent years, there has been an increase in CFT infestations outside of the permanent quarantine area in Texas. Nilgai are of interest in understanding how CFT may be spread through the landscape. Thirty nilgai of both sexes were captured and fitted with satellite radio collars in South Texas to gain information about movement patterns, response to disturbances, and movement barriers. Median annual home range sizes were highly variable in males (4665ha, range=571-20,809) and females (1606ha, range=848-29,909). Female movement patterns appeared to be seasonal with peaks during June-August; these peaks appeared to be a function of break-ups in female social groups rather than environmental conditions. Nilgai, which reportedly are sensitive to disturbance, were more likely to relocate into new areas immediately after being captured versus four other types of helicopter activities. Nilgai did not cross 1.25m high cattle fences parallel to paved highways but did cross other fence types. Results indicate that females have a higher chance of spreading CFT through the landscape than males, but spread of CFT may be mitigated via maintenance of cattle fences running parallel with paved highways. Our results highlight the importance of documenting species-specific behavior in wildlife-livestock interfaces that can be used to develop effective disease management strategies in the United States and worldwide.

Molecular Comparison of Cattle Fever Ticks from Native and Introduced Ranges, with Insights into Optimal Search Areas for Classical Biological Control Agents

Abstract. Cattle fever ticks, the southern cattle tick, Rhipicephalus microplus (Canestrini), and cattle tick, Rhipicephalus annulatus (Say), are livestock pests endemic to Mexico and invasive along the Texas-Mexico border. Resistance to acaricide, alternate wildlife hosts, and pathogenic landscape-forming weeds present challenges for sustainable eradication of this pest in the U.S. Classical biological control is being explored as a strategy to control cattle fever ticks, especially on alternate hosts such as nilgai antelope, Boselaphus tragocamelus (Pallas), and white-tailed deer, Odocoileus virginianus (Zimmermann). Molecular genetic tools were used to compare populations of cattle fever ticks from native and introduced ranges to provide insights into optimal search areas for potential biological control agents. Accessions representative of invasive populations of southern cattle tick from subtropical Zapata, TX, and other parts of the invaded range including Brazil and Kenya matched most closely populations in Cambodia and the Philippines. Similarly, accessions of cattle tick from invaded range in Del Rio, TX matched closely with accessions from native range in Bulgaria and Romania. These regions should be prioritized for field exploration for biological control agents.