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Current Limitations in the Control and Spread of Ticks that Affect Livestock: A Review
Agustín Estrada-Pea,Mo Salman
Agriculture , 2013, DOI: 10.3390/agriculture3020221
Abstract: Ticks are well-known parasites that affect livestock productivity. This paper reviews the current knowledge regarding the spread of ticks with their impact in animal health and the limitations to achieve effective control measures. The forecasted trends in climate play an obvious role in promoting the spread of ticks in several regions. It appears that climate warming is pivotal in the spread and colonization of new territories by Rhipicephalus microplus in several regions of Africa. The reported increase in altitude of this tick species in the mountainous regions of Central and South America appears to be driven by such general trends in climate change. This factor, however, is not the only single contributor to the spread of ticks. The poor management of farms, uncontrolled movements of domestic animals, abundance of wild animals, and absence of an adequate framework to capture the ecological plasticity of certain ticks may explain the complexity of the control measures. In this paper, we review several details regarding the relationships of ticks with the environment, wild fauna and competition with other species of ticks. Our intention is to highlight these relationships with the aim to produce a coherent framework to explore tick ecology and its relationship with animal production systems.
Impact of Climate Trends on Tick-Borne Pathogen Transmission
Agustín Estrada-Pea,José de la Fuente
Frontiers in Physiology , 2012, DOI: 10.3389/fphys.2012.00064
Abstract: Recent advances in climate research together with a better understanding of tick–pathogen interactions, the distribution of ticks and the diagnosis of tick-borne pathogens raise questions about the impact of environmental factors on tick abundance and spread and the prevalence and transmission of tick-borne pathogens. While undoubtedly climate plays a role in the changes in distribution and seasonal abundance of ticks, it is always difficult to disentangle factors impacting on the abundance of tick hosts from those exerted by human habits. All together, climate, host abundance, and social factors may explain the upsurge of epidemics transmitted by ticks to humans. Herein we focused on tick-borne pathogens that affect humans with epidemic potential. Borrelia burgdorferi s.l. (Lyme disease), Anaplasma phagocytophilum (human granulocytic anaplasmosis), and tick-borne encephalitis virus (tick-borne encephalitis) are transmitted by Ixodes spp. Crimean–Congo hemorrhagic fever virus (Crimean–Congo hemorrhagic fever) is transmitted by Hyalomma spp. In this review, we discussed how vector tick species occupy the habitat as a function of different climatic factors, and how these factors impact on tick survival and seasonality. How molecular events at the tick–pathogen interface impact on pathogen transmission is also discussed. Results from statistically and biologically derived models are compared to show that while statistical models are able to outline basic information about tick distributions, biologically derived models are necessary to evaluate pathogen transmission rates and understand the effect of climatic variables and host abundance patterns on pathogen transmission. The results of these studies could be used to build early alert systems able to identify the main factors driving the subtle changes in tick distribution and seasonality and the prevalence of tick-borne pathogens.
Modeling the Impact of Climate and Landscape on the Efficacy of White Tailed Deer Vaccination for Cattle Tick Control in Northeastern Mexico
Agustín Estrada-Pea, Diana Carreón, Consuelo Almazán, José de la Fuente
PLOS ONE , 2014, DOI: 10.1371/journal.pone.0102905
Abstract: Cattle ticks are distributed worldwide and affect animal health and livestock production. White tailed deer (WTD) sustain and spread cattle tick populations. The aim of this study was to model the efficacy of anti-tick vaccination of WTD to control tick infestations in the absence of cattle vaccination in a territory where both host species coexist and sustain cattle tick populations. Agent-based models that included land cover/landscape properties (patch size, distances to patches) and climatic conditions were built in a GIS environment to simulate WTD vaccine effectiveness under conditions where unvaccinated cattle shared the landscape. Published and validated information on tick life cycle was used to build models describing tick mortality and developmental rates. Data from simulations were applied to a large territory in northeastern Mexico where cattle ticks are endemic and WTD and cattle share substantial portions of the habitat. WTD movements were simulated together with tick population dynamics considering the actual landscape and climatic features. The size of the vegetation patches and the distance between patches were critical for the successful control of tick infestations after WTD vaccination. The presence of well-connected, large vegetation patches proved essential for tick control, since the tick could persist in areas of highly fragmented habitat. The continued application of one yearly vaccination on days 1-70 for three years reduced tick abundance/animal/patch by a factor of 40 and 60 for R. annulatus and R. microplus, respectively when compared to non-vaccinated controls. The study showed that vaccination of WTD alone during three consecutive years could result in the reduction of cattle tick populations in northeastern Mexico. Furthermore, the results of the simulations suggested the possibility of using vaccines to prevent the spread and thus the re-introduction of cattle ticks into tick-free areas.
Occurrence Patterns of Afrotropical Ticks (Acari: Ixodidae) in the Climate Space Are Not Correlated with Their Taxonomic Relationships
Agustín Estrada-Pea, Adrián Estrada-Sánchez, David Estrada-Sánchez
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0036976
Abstract: Foci of tick species occur at large spatial scales. They are intrinsically difficult to detect because the effect of geographical factors affecting conceptual influence of climate gradients. Here we use a large dataset of occurrences of ticks in the Afrotropical region to outline the main associations of those tick species with the climate space. Using a principal components reduction of monthly temperature and rainfall values over the Afrotropical region, we describe and compare the climate spaces of ticks in a gridded climate space. The dendrogram of distances among taxa according to occurrences in the climate niche is used to draw functional groups, or clusters of species with similar occurrences in the climate space, as different from morphologically derived (taxonomical) groups. We aim to further define the drivers of species richness and endemism at such a grid as well as niche similarities (climate space overlap) among species. Groups of species, as defined from morphological traits alone, are uncorrelated with functional clusters. Taxonomically related species occur separately in the climate gradients. Species belonging to the same functional group share more niche among them than with species in other functional groups. However, niche equivalency is also low for species within the same taxonomic cluster. Thus, taxa evolving from the same lineage tend to maximize the occupancy of the climate space and avoid overlaps with other species of the same taxonomic group. Richness values are drawn across the gradient of seasonal variation of temperature, higher values observed in a portion of the climate space with low thermal seasonality. Richness and endemism values are weakly correlated with mean values of temperature and rainfall. The most parsimonious explanation for the different taxonomic groups that exhibit common patterns of climate space subdivision is that they have a shared biogeographic history acting over a group of ancestrally co-distributed organisms.
Evidence of the Importance of Host Habitat Use in Predicting the Dilution Effect of Wild Boar for Deer Exposure to Anaplasma spp
Agustín Estrada-Pea, Pelayo Acevedo, Francisco Ruiz-Fons, Christian Gortázar, José de la Fuente
PLOS ONE , 2008, DOI: 10.1371/journal.pone.0002999
Abstract: Foci of tick-borne pathogens occur at fine spatial scales, and depend upon a complex arrangement of factors involving climate, host abundance and landscape composition. It has been proposed that the presence of hosts that support tick feeding but not pathogen multiplication may dilute the transmission of the pathogen. However, models need to consider the spatial component to adequately explain how hosts, ticks and pathogens are distributed into the landscape. In this study, a novel, lattice-derived, behavior-based, spatially-explicit model was developed to test how changes in the assumed perception of different landscape elements affect the outcome of the connectivity between patches and therefore the dilution effect. The objective of this study was to explain changes in the exposure rate (ER) of red deer to Anaplasma spp. under different configurations of suitable habitat and landscape fragmentation in the presence of variable densities of the potentially diluting host, wild boar. The model showed that the increase in habitat fragmentation had a deep impact on Habitat Sharing Ratio (HSR), a parameter describing the amount of habitat shared by red deer and wild boar, weighted by the probability of the animals to remain together in the same patch (according to movement rules), the density of ticks and the density of animals at a given vegetation patch, and decreased the dilution effect of wild boar on deer Anaplasma ER. The model was validated with data collected on deer, wild boar and tick densities, climate, landscape composition, host vegetation preferences and deer seropositivity to Anaplasma spp. (as a measure of ER) in 10 study sites in Spain. However, although conditions were appropriate for a dilution effect, empirical results did not show a decrease in deer ER in sites with high wild boar densities. The model showed that the HSR was the most effective parameter to explain the absence of the dilution effect. These results suggest that host habitat usage may weaken the predicted dilution effect for tick-borne pathogens and emphasize the importance of the perceptual capabilities of different hosts in different landscapes and habitat fragmentation conditions for predictions of dilution effects.
The Influence of Interspecific Competition and Host Preference on the Phylogeography of Two African Ixodid Tick Species
Nídia Cangi, Ivan G. Horak, Dmitry A. Apanaskevich, Sonja Matthee, Luís C. B. G. das Neves, Agustín Estrada-Pea, Conrad A. Matthee
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0076930
Abstract: A comparative phylogeographic study on two economically important African tick species, Amblyomma hebraeum and Hyalomma rufipes was performed to test the influence of host specificity and host movement on dispersion. Pairwise AMOVA analyses of 277 mtDNA COI sequences supported significant population differentiation among the majority of sampling sites. The geographic mitochondrial structure was not supported by nuclear ITS-2 sequencing, probably attributed to a recent divergence. The three-host generalist, A. hebraeum, showed less mtDNA geographic structure, and a lower level of genetic diversity, while the more host-specific H. rufipes displayed higher levels of population differentiation and two distinct mtDNA assemblages (one predominantly confined to South Africa/Namibia and the other to Mozambique and East Africa). A zone of overlap is present in southern Mozambique. A mechanistic climate model suggests that climate alone cannot be responsible for the disruption in female gene flow. Our findings furthermore suggest that female gene dispersal of ticks is more dependent on the presence of juvenile hosts in the environment than on the ability of adult hosts to disperse across the landscape. Documented interspecific competition between the juvenile stages of H. rufipes and H. truncatum is implicated as a contributing factor towards disrupting gene flow between the two southern African H. rufipes genetic assemblages.
Allopatric speciation in ticks: genetic and reproductive divergence between geographic strains of Rhipicephalus (Boophilus) microplus
Marcelo B Labruna, Victoria Naranjo, Atilio J Mangold, Carolina Thompson, Agustín Estrada-Pea, Alberto A Guglielmone, Frans Jongejan, José de la Fuente
BMC Evolutionary Biology , 2009, DOI: 10.1186/1471-2148-9-46
Abstract: The results showed that the crosses between Australian and Argentinean or Mozambican strains of boophilid ticks are infertile while crosses between Argentinean and Mozambican strains are fertile. These results showed that tick strains from Africa (Mozambique) and America (Argentina) are the same species, while ticks from Australia may actually represent a separate species. The genetic analysis of mitochondrial 12S and 16S rDNA and microsatellite loci were not conclusive when taken separately, but provided evidence that Australian tick strains were genetically different from Asian, African and American strains.The results reported herein support the hypothesis that at least two different species share the name R. microplus. These species could be redefined as R. microplus (Canestrini, 1887) (for American and African strains) and probably the old R. australis Fuller, 1899 (for Australian strains), which needs to be redescribed. However, experiments with a larger number of tick strains from different geographic locations are needed to corroborate these results.The cattle tick, Rhipicephalus (Boophilus) microplus, is distributed in tropical and subtropical regions of the world [1]. Infestations with R. microplus economically impact cattle industry by reducing weight gain and milk production, and by transmitting pathogens that cause babesiosis (Babesia bovis and B. bigemina) and anaplasmosis (Anaplasma marginale) [2,3]. The morphological and genetic differences among R. microplus strains have been documented in the literature [4,5]. Although Londt and Arthur [6] argued that morphological differences between these strains are too slight to warrant species status, other results provided opposing evidence [7]. These authors demonstrated that hybrids resulting from crossing R. (B.) microplus strains from South Africa and Australia were sterile. Thus, R. microplus from South Africa and Australia might be regarded as different species [8].Contradictory results have been report
Phylogeographic analysis reveals association of tick-borne pathogen, Anaplasma marginale, MSP1a sequences with ecological traits affecting tick vector performance
Agustín Estrada-Pea, Victoria Naranjo, Karina Acevedo-Whitehouse, Atilio J Mangold, Katherine M Kocan, José de la Fuente
BMC Biology , 2009, DOI: 10.1186/1741-7007-7-57
Abstract: In this study we showed that the phylogeography of A. marginale MSP1a sequences is associated with world ecological regions (ecoregions) resulting in different evolutionary pressures and thence MSP1a sequences. The results demonstrated that the MSP1a first (R1) and last (RL) repeats and microsatellite sequences were associated with world ecoregion clusters with specific and different environmental envelopes. The evolution of R1 repeat sequences was found to be under positive selection. It is hypothesized that the driving environmental factors regulating tick populations could act on the selection of different A. marginale MSP1a sequence lineages, associated to each ecoregion.The results reported herein provided the first evidence that the evolution of A. marginale was linked to ecological traits affecting tick vector performance. These results suggested that some A. marginale strains have evolved under conditions that support pathogen biological transmission by R. microplus, under different ecological traits which affect performance of R. microplus populations. The evolution of other A. marginale strains may be linked to transmission by other tick species or to mechanical transmission in regions where R. microplus is currently eradicated. The information derived from this study is fundamental toward understanding the evolution of other vector-borne pathogens.The genus Anaplasma (Rickettsiales: Anaplasmataceae) contains obligate intracellular organisms found exclusively within membrane-bound inclusions or parasitophorous vacuoles in the cytoplasm of both vertebrate and invertebrate host cells [1,2]. The genus Anaplasma includes pathogens of ruminants, A. marginale, A. centrale, A. bovis, and A. ovis. Also included in this genus are A. phagocytophilum, which infects a wide range of hosts including humans and wild and domesticated animals, and A. platys that infects dogs.To date, most research has been reported for A. marginale, the type species for the genus Anaplasma
Rickettsia parkeri: a Rickettsial pathogen transmitted by ticks in endemic areas for spotted fever rickettsiosis in southern Uruguay
Venzal, José M.;Estrada-Pea, Agustín;Portillo, Aránzazu;Mangold, Atilio J.;Castro, Oscar;Souza, Carlos G. De;Félix, María L.;Pérez-Martínez, Laura;Santibánez, Sonia;Oteo, José A.;
Revista do Instituto de Medicina Tropical de S?o Paulo , 2012, DOI: 10.1590/S0036-46652012000300003
Abstract: at first rickettsia conorii was implicated as the causative agent of spotted fever in uruguay diagnosed by serological assays. later rickettsia parkeri was detected in human-biting amblyomma triste ticks using molecular tests. the natural vector of r. conorii, rhipicephalus sanguineus, has not been studied for the presence of rickettsial organisms in uruguay. to address this question, 180 r. sanguineus from dogs and 245 a. triste from vegetation (flagging) collected in three endemic localities were screened for spotted fever group (sfg) rickettsiosis in southern uruguay. tick extracted dna pools were subjected to pcr using primers which amplify a fragment of the rickettsial glta gene. positive tick dna pools with these primers were subjected to a second pcr round with primers targeting a fragment of the ompa gene, which is only present in sfg rickettsiae. no rickettsial dna was detected in r. sanguineus. however, dna pools of a. triste were found to be positive for a rickettsial organism in two of the three localities, with prevalences of 11.8% to 37.5% positive pools. dna sequences generated from these pcr-positive ticks corresponded to r. parkeri. these findings, joint with the aggressiveness shown by a. triste towards humans, support previous data on the involvement of a. triste as vector of human infections caused by r. parkeri in uruguay.
Functional and Immunological Relevance of Anaplasma marginale Major Surface Protein 1a Sequence and Structural Analysis
Alejandro Cabezas-Cruz, Lygia M. F. Passos, Katarzyna Lis, Rachel Kenneil, James J. Valdés, Joana Ferrolho, Miray Tonk, Anna E. Pohl, Libor Grubhoffer, Erich Zweygarth, Varda Shkap, Mucio F. B. Ribeiro, Agustín Estrada-Pea, Katherine M. Kocan, José de la Fuente
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0065243
Abstract: Bovine anaplasmosis is caused by cattle infection with the tick-borne bacterium, Anaplasma marginale. The major surface protein 1a (MSP1a) has been used as a genetic marker for identifying A. marginale strains based on N-terminal tandem repeats and a 5′-UTR microsatellite located in the msp1a gene. The MSP1a tandem repeats contain immune relevant elements and functional domains that bind to bovine erythrocytes and tick cells, thus providing information about the evolution of host-pathogen and vector-pathogen interactions. Here we propose one nomenclature for A. marginale strain classification based on MSP1a. All tandem repeats among A. marginale strains were classified and the amino acid variability/frequency in each position was determined. The sequence variation at immunodominant B cell epitopes was determined and the secondary (2D) structure of the tandem repeats was modeled. A total of 224 different strains of A. marginale were classified, showing 11 genotypes based on the 5′-UTR microsatellite and 193 different tandem repeats with high amino acid variability per position. Our results showed phylogenetic correlation between MSP1a sequence, secondary structure, B-cell epitope composition and tick transmissibility of A. marginale strains. The analysis of MSP1a sequences provides relevant information about the biology of A. marginale to design vaccines with a cross-protective capacity based on MSP1a B-cell epitopes.
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