Simulation of climate‐tick‐host‐landscape interactions: Effects of shifts in the seasonality of host population fluctuations on tick densities

Tick vector systems are comprised of complex climate‐tick‐host‐landscape interactions that are difficult to identify and estimate from empirical observations alone. We developed a spatially‐explicit, individual‐based model, parameterized to represent ecological conditions typical of the south‐central United States, to examine effects of shifts in the seasonal occurrence of fluctuations of host densities on tick densities. Simulated shifts in the seasonal occurrence of periods of high and low host densities affected both the magnitude of unfed tick densities and the seasonality of tick development. When shifting the seasonal densities of all size classes of hosts (small, medium, and large) synchronously, densities of nymphs were affected more by smaller shifts away from the baseline host seasonality than were densities of larval and adult life stages. When shifting the seasonal densities of only a single size‐class of hosts while holding other size classes at their baseline levels, densities of larval, nymph, and adult life stages responded differently. Shifting seasonal densities of any single host‐class earlier resulted in a greater increase in adult tick density than when seasonal densities of all host classes were shifted earlier simultaneously. The mean densities of tick life stages associated with shifts in host densities resulted from system‐level interactions of host availability with tick phenology. For example, shifting the seasonality of all hosts ten weeks earlier resulted in an approximately 30% increase in the relative degree of temporal co‐occurrence of actively host‐seeking ticks and hosts compared to baseline, whereas shifting the seasonality of all hosts ten weeks later resulted in an approximately 70% decrease compared to baseline. Differences among scenarios in the overall presence of active host‐seeking ticks in the system were due primarily to the degree of co‐occurrence of periods of high densities of unfed ticks and periods of high densities of hosts.     

Abundance and seasonal activity of questing Ixodes ricinus ticks in their natural habitats in southern Germany in 2011

Questing ticks were sampled monthly over a period of 11 months from February, 2011 to December, 2011 at 13 sites in southern Germany using the flagging method. The ticks were identified to species, gender, and stadium. Although both I. ricinus and D. reticulatus were sampled, this study concentrated on I. ricinus, since it was the most abundant tick to be found. Additional weather data (air and soil temperature, relative air humidity, precipitation, sunshine duration) were recorded on each sampling site and the local vegetation described. A total of 14, 394 ticks was collected (7,862 larvae, 5,568 nymphs, 964 adults) and their activity was recorded in order to determine the seasonal activity pattern over different periods of the year. In contrast to the widely accepted pattern of a bimodal seasonal activity in moderate areas with a dominant peak in spring and a minor peak in autumn, a unimodal activity pattern was found for all development stages on six of the 12 sampling sites. Tick abundance was compared to weather variables. Tick host‐seeking activity was found to be significantly dependent on the temperature at ground level, precipitation, and sunshine duration as well as relative air humidity. Adult ticks showed a positive correlation with the duration of sunshine, whereas nymphs were mostly unaffected by this phenomenon.     

Seasonal and diel activity of Ixodes ricinus (Acari: Ixodidae) subpopulations in Denmark. Aspects of size, physiological age, and malate dehydrogenase genotype in a forest site without any undergrowth

The underlying population dynamics and the behavioural patterns of the vectors are key issues in understanding the transmission of vector borne pathogens. For the tick Ixodes ricinus both seasonal and diel activity have been described as bimodal patterns, which in seasonal aspect has been interpreted as representing two cohorts. However, recent studies have shown that this interpretation may be incorrect. The aim of this study was to obtain more detailed information on nymph host seeking by studying subpopulations of ticks during the day and season. The study was designed to allow for comparisons of the diel variation and seasonal variation in their dependency in a number of tick characteristics. The study took place in a forest with planted beech trees without any undergrowth. Ticks were collected by flagging the dead leaves on the forest floor. For each nymph, a number of visual observations were made. The size and physiological age was observed and the nymphs were genotyped in the malate dehydrogenase locus (MDH, E.C. 1.1.1.37). Briefly the main results can be given as: (i) There were significant differences in the composition of size classes during the season, but only limited trends in time. (ii) The proportion of the small nymphs was highly variable, with a variation from 3% to 24% in October and September, respectively. (iii) The diel variation in MDH genotypes was significant in May and August. (iv) Nymph size classes and physiological age appeared to interact. The non-random interaction was caused by a relatively even distribution of small nymphs in all four age classes, while large nymphs tended to fall into age class 2 and 3. The length by age interaction for the individual months was noted to be significant in May, July, August and September, but not in June. Similarly the interaction was significant in the morning and afternoon, but not at midday. The overall results describe the seasonal and diel activity patterns as changing systematically for several characteristics under the influence of weather condition and population dynamics. In conclusion: The observations are best interpreted as being produced of a single cohort of ticks, but the revealed complexity of the host seeking activity suggest that measures of activity × abundance should be interpreted very cautiously in relation to population dynamics. This revised version was published online in July 2006 with corrections to the Cover Date.     

Seasonal and geographical distribution of adult Ixodes scapularis say (Acari: Ixodidae) in Louisiana.

The distribution and seasonality of adult black-legged ticks (Ixodes scapularis Say) in Louisiana was measured. The presence of adult ticks was determined by flagging at 106 sites throughout Louisiana. It was concluded that Ixodes scapularis is widely distributed throughout Louisiana. Ticks were also collected twice per month at one site over a 15-month period by flagging and use of CO2 traps to establish the relative seasonal abundance pattern of free-living adult ticks. Host-seeking, black-legged adult ticks were collected from October to May. Peak adult abundance was observed in December. More ticks were collected by the use of CO2 traps compared to flagging in October, November, and February. No black-legged tick larvae or nymphs were collected in this study using either collection method.     

Seasonal and diel activity of Ixodes ricinus (Acari: Ixodidae) subpopulations in Denmark. Aspects of size, physiological age, and malate dehydrogenase genotype in a forest site without any undergrowth

The underlying population dynamics and the behavioural patterns of the vectors are key issues in understanding the transmission of vector borne pathogens. For the tick Ixodes ricinus both seasonal and diel activity have been described as bimodal patterns, which in seasonal aspect has been interpreted as representing two cohorts. However, recent studies have shown that this interpretation may be incorrect. The aim of this study was to obtain more detailed information on nymph host seeking by studying subpopulations of ticks during the day and season. The study was designed to allow for comparisons of the diel variation and seasonal variation in their dependency in a number of tick characteristics. The study took place in a forest with planted beech trees without any undergrowth. Ticks were collected by flagging the dead leaves on the forest floor. For each nymph, a number of visual observations were made. The size and physiological age was observed and the nymphs were genotyped in the malate dehydrogenase locus (MDH, E.C. 1.1.1.37). Briefly the main results can be given as: (i) There were significant differences in the composition of size classes during the season, but only limited trends in time. (ii) The proportion of the small nymphs was highly variable, with a variation from 3% to 24% in October and September, respectively. (iii) The diel variation in MDH genotypes was significant in May and August. (iv) Nymph size classes and physiological age appeared to interact. The non-random interaction was caused by a relatively even distribution of small nymphs in all four age classes, while large nymphs tended to fall into age class 2 and 3. The length by age interaction for the individual months was noted to be significant in May, July, August and September, but not in June. Similarly the interaction was significant in the morning and afternoon, but not at midday. The overall results describe the seasonal and diel activity patterns as changing systematically for several characteristics under the influence of weather condition and population dynamics. In conclusion: The observations are best interpreted as being produced of a single cohort of ticks, but the revealed complexity of the host seeking activity suggest that measures of activity x abundance should be interpreted very cautiously in relation to population dynamics.     

Comparison of flagging,walking, trapping,and collecting from hosts as sampling methods for northern deer ticks,Ixodes dammini,and lone-star ticks,Amblyomma americanum (Acari: Ixodidae)

Ticks were sampled by flagging, collecting from the investigator's clothing (walking samples), trapping with dry-ice bait, and collecting from mammal hosts on Fire Island, NY, U.S.A. The habitat distribution of adult deer ticks,Ixodes dammini, was the same in simultaneous collections from the investigator's clothing and from muslin flags. Walking and flagging samples can both be biased by differences between investigators, so the same person should do comparative samples whenever possible. Walking samples probably give a more accurate estimate than flagging samples of the human risk of encountering ticks. However, ticks (such as immatureI. dammini) that seek hosts in leaf litter and ground-level vegetation are poorly sampled by walking collections. These ticks can be sampled by flagging at ground level.Dry-ice-baited tick-traps caught far more lone-star ticks,Amblyomma americanum, than deer ticks, even in areas where deer ticks predominated in flagging samples. In comparisons of tick mobility in the lab, nymphalA. americanum were more mobile than nymphalI. dammini in 84% of the trials. Therefore, the trapping bias may result from increased trap encounter due to more rapid movement byA. americanum, although greater attraction to carbon dioxide may also play a role. Tick traps are useful for intraspecific between-habitat comparisons.Early in their seasonal activity period, larvalI. dammini were better represented in collections from mouse hosts than in flagging samples. Apparently, sampling from favored hosts can detect ticks at low population levels, but often cannot be used to get accurate estimates of pathogen prevalence in questing ticks.     

Persistence of Pathogens with Short Infectious Periods in Seasonal Tick Populations: The Relative Importance of Three Transmission Routes

Background

The flaviviruses causing tick-borne encephalitis (TBE) persist at low but consistent levels in tick populations, despite short infectious periods in their mammalian hosts and transmission periods constrained by distinctly seasonal tick life cycles. In addition to systemic and vertical transmission, cofeeding transmission has been proposed as an important route for the persistence of TBE-causing viruses. Because cofeeding transmission requires ticks to feed simultaneously, the timing of tick activity may be critical to pathogen persistence. Existing models of tick-borne diseases do not incorporate all transmission routes and tick seasonality. Our aim is to evaluate the influence of seasonality on the relative importance of different transmission routes by using a comprehensive mathematical model.

Methodology/Principal Findings

We developed a stage-structured population model that includes tick seasonality and evaluated the relative importance of the transmission routes for pathogens with short infectious periods, in particular Powassan virus (POWV) and the related “deer tick virus,” emergent encephalitis-causing flaviviruses in North America. We used the next generation matrix method to calculate the basic reproductive ratio and performed elasticity analyses. We confirmed that cofeeding transmission is critically important for such pathogens to persist in seasonal tick populations over the reasonable range of parameter values. At higher but still plausible rates of vertical transmission, our model suggests that vertical transmission can strongly enhance pathogen prevalence when it operates in combination with cofeeding transmission.

Conclusions/Significance

Our results demonstrate that the consistent prevalence of POWV observed in tick populations could be maintained by a combination of low vertical, intermediate cofeeding and high systemic transmission rates. When vertical transmission is weak, nymphal ticks support integral parts of the transmission cycle that are critical for maintaining the pathogen. We also extended the model to pathogens that cause chronic infections in hosts and found that cofeeding transmission could contribute to elevating prevalence even in these systems. Therefore, the common assumption that cofeeding transmission is not relevant in models of chronic host infection, such as Lyme disease, could lead to underestimating pathogen prevalence.     

The role of host management in tick population changes on Rusinga Island,Kenya

Contrary to patterns described elsewhere, tick numbers on Rusinga Island cattle drop markedly after the onset of the rainy season. One possible explanation is that this is related to seasonal differences in host behaviour since cattle grazing on the island are restricted during the crop-growing season (the rainy season) and free grazing afterwards. In a field experiment, cattle were divided into two groups, free grazing and restricted, for 2 months each during the rainy season and during the dry season, and the number of ticks infesting each group was compared. In both seasons, the free-grazing group carried more ticks than the restricted group. Not only did the restricted group come into less contact with ticks, they were also exposed to tick-predating chickens for longer periods each day than the free-grazing group. Management practices that affect host behaviour should, therefore, be taken into consideration in tick population studies.     

Correlation of Borrelia burgdorferi sensu lato prevalence in questing Ixodes ricinus ticks with specific abiotic traits in the western palearctic

This meta-analysis of reports examining ticks throughout the Western Palearctic region indicates a distinct geographic pattern for Borrelia burgdorferi sensu lato prevalence in questing nymphal Ixodes ricinus ticks. The greatest prevalence was reported between the 5°E and 25°E longitudes based on an analysis of 123 collection points with 37,940 nymphal tick specimens (87.43% of total nymphs; 56.35% of total ticks in the set of reports over the target area). Climatic traits, such as temperature and vegetation stress, and their seasonality correlated with Borrelia prevalence in questing ticks. The greatest prevalence was associated with mild winter, high summer, and low seasonal amplitude of temperatures within the range of the tick vector, higher vegetation indices in the May-June period, and well-connected vegetation patches below a threshold at which rates suddenly drop. Classification of the target territory using a qualitative risk index derived from the abiotic variables produced an indicator of the probability of finding infected ticks in the Western Palearctic region. No specific temporal trends were detected in the reported prevalence. The ranges of the different B. burgdorferi sensu lato genospecies showed a pattern of high biodiversity between 4°W and 20°E, partially overlapping the area of highest prevalence in ticks. Borrelia afzelii and Borrelia garinii are the dominant species in central Europe (east of ～25°E), but B. garinii may appear alone at southern latitudes and Borrelia lusitaniae is the main indicator species for meridional territories.     

Impact of biodiversity and seasonality on Lyme-pathogen transmission

Lyme disease imposes increasing global public health challenges. To better understand the joint effects of seasonal temperature variation and host community composition on the pathogen transmission, a stage-structured periodic model is proposed by integrating seasonal tick development and activity, multiple host species and complex pathogen transmission routes between ticks and reservoirs. Two thresholds, one for tick population dynamics and the other for Lyme-pathogen transmission dynamics, are identified and shown to fully classify the long-term outcomes of the tick invasion and disease persistence. Seeding with the realistic parameters, the tick reproduction threshold and Lyme disease spread threshold are estimated to illustrate the joint effects of the climate change and host community diversity on the pattern of Lyme disease risk. It is shown that climate warming can amplify the disease risk and slightly change the seasonality of disease risk. Both the “dilution effect” and “amplification effect” are observed by feeding the model with different possible alternative hosts. Therefore, the relationship between the host community biodiversity and disease risk varies, calling for more accurate measurements on the local environment, both biotic and abiotic such as the temperature and the host community composition.     

Detection of Alpha and Gamma-Proteobacteria in <Emphasis Type="Italic">Amblyomma triste</Emphasis> (Acari: Ixodidae) from Uruguay

Amblyomma triste is the most prevalent tick species reported in human tick bites in Uruguay and has been found to be infected with Rickettsia parkeri, but no other microorganisms have been reported from this tick. A sample of 254 adults of A. triste was collected by flagging on vegetation in suburban areas in southern Uruguay. Pools of five ticks were assembled and a screening for the DNA from the resulting 51 pools was realized by PCR assays using primers for amplifying a fragment of 16S rRNA gene for members of Anaplasmataceae. Seventeen pools were positive (33%) and the sequenciation of the gene fragment amplified revealed the presence of a putative new Alpha-Proteobacterium (denominated Atri-uru). The phylogenetic analysis showed that this microorganism is closely related to the symbiont of I. ricinus denominated ‘Candidatus Midichloria mitochondrii’ and other associated organisms. This rickettsial symbiont of ticks is included in a recent new clade proposed for the Alpha subclass of the Proteobacteria. The discovery of this bacterium in A. triste is the first evidence of this group of Rickettsiales detected in the Genus Amblyomma, and the first record in South America. Also, in two of 17 positive samples a Gamma-Proteobacterium related to Francisella-like organisms was detected.     

Forest floor respiration in a black spruce taiga forest ecosystem in Alaska

A technique was developed for measuring respiration of virtually undisturbed forest floor samples, and used to follow seasonal changes in two black spruce forest stands in interior Alaska, In the laboratory, soil respiration showed a positive response to increasing temperature: however, respiration measured in the field was negatively correlated with air and soil temperature, but positively correlated with water content of the soil within the range (100–250% of dry weight) normally experienced in the field. Moisture levels above 250% inhibited respiration. Precipitation events usually stimulate forest floor respiration, but prolonged periods of dry and rainy weather lead to limitation of respiration by sub- and supraoptimal moisture, respectively. Long-term confinement of soil has significant effects upon soil arthropod densities, moisture content, temperature, and respiration, and should not be taken to represent the natural conditions of the forest floor.     

Understanding the Relationships between Landscape Connectivity and Abundance of Ixodes ricinus Ticks

The density of Ixodes ricinus ticks in a heterogeneous landscape of northern Spain was determined and associated with some aspects of habitat topology. The habitat mosaic was used to quantify connectivity between patches of different tick density. The analysis revealed that patches with high tick abundance are ‘stepping-stone’ territories that, when removed from the landscape, cause large changes in connectivity. Sites with medium tick abundance do not cause such a critical transition in connectivity. Patches with low tick abundance, but optimal abiotic conditions for survival are located within the minimum cost corridors network joining the patches, while those sites where the tick has been intermittently collected are located at variable distances from this network. These results suggest that tick distribution in a zone is highly affected not only by abiotic variables (vegetation and weather) but also by host movements. Whether these high-density ‘stepping-stone’ patches occur in other tick species needs to be evaluated because of the potential implications of these foci for human health. This revised version was published online in July 2006 with corrections to the Cover Date.     

Modelling the transmission dynamics of Theileria annulata: model structure and validation for the Turkish context

A mathematical model that describes the transmission dynamics of Theileria annulata is proposed that consists of 2 host components: the Hyalomma tick population and a compartmental model of T. annulata infection in the cattle population. The model was parameterized using data describing tick infestation and the infection status of cattle in Turkey from 2006 to 2008. The tick attachment rates are highly seasonal and because of the temporal separation of infectious and susceptible ticks virtually all ticks are infected by carrier cattle, so that annual peaks of disease in cattle do not impact on infection in the Hyalomma tick population. The impact of intervention measures that target the tick population both on the host and in the environment and their impact on the transmission of T. annulata were investigated. Interventions that have a limited 'one-off' impact and interventions that have a more permanent impact were both considered. The results from the model show the importance of targeting ticks during the period when they have left their first host as nymphs but have yet to feed on their second host.     

Species,developmental stage and infection with microbial pathogens of engorged ticks removed from dogs and questing ticks

Research into tick‐borne diseases implies vector sampling and the detection and identification of microbial pathogens. Ticks were collected simultaneously from dogs that had been exposed to tick bites and by flagging the ground in the area in which the dogs had been exposed. In total, 200 ticks were sampled, of which 104 came from dogs and 96 were collected by flagging. These ticks were subsequently examined for DNA of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Rickettsia spp. and Babesia canis. A mixed sample of adult ticks and nymphs of Ixodes ricinus (Ixodida: Ixodidae) and Haemaphysalis concinna (Ixodida: Ixodidae) was obtained by flagging. Female I. ricinus and adult Dermacentor reticulatus (Ixodida: Ixodidae) ticks dominated the engorged ticks removed from dogs. Rickettsia spp. were detected in 17.0% of the examined ticks, A. phagocytophilum in 3.5%, B. canis in 1.5%, and B. burgdorferi s.l. in 16.0%. Ticks with multiple infections were found only among the flagging sample. The ticks removed from the dogs included 22 infected ticks, whereas the flagging sample included 44 infected ticks. The results showed that the method for collecting ticks influences the species composition of the sample and enables the detection of a different pattern of pathogens. Sampling strategies should be taken into consideration when interpreting studies on tick‐borne pathogens.     

Ecological characterization of a tick community across a landscape gradient exhibiting differential anthropogenic disturbance in the Atlantic Forest ecoregion in Argentina

An ecological analysis of a tick (Ixodida: Ixodidae) community across a landscape gradient presenting differential anthropogenic disturbance in the Atlantic Forest ecoregion in Argentina was performed. Ticks were collected from vegetation and hosts between September 2014 and August 2016. A total of 12 697 free‐living ticks and 3347 specimens from hosts were collected, including 317 ticks infesting humans. The values obtained show considerable species diversity in the forest environment accompanied by low equitability. The similarity index derived from a comparison of forest and agricultural environments was higher than that calculated by comparing forest and urban environments. The data suggest that although a cycle of one generation per year is apparent in some species, more than one cohort may co‐exist within the populations of some of these species. Well‐marked patterns of the seasonal distribution of free‐living tick species emerged in environments with no anthropic modification. The results indicate that forest environments are more suitable habitats than agricultural and urban environments for many species of native tick, but are unsuitable for exotic species that have successfully established in environments that have been modified by man.     

Attachment site selection of ticks on roe deer, <Emphasis Type="Italic">Capreolus capreolus</Emphasis>

The spatio-temporal attachment site patterns of ticks feeding on their hosts can be of significance if co-feeding transmission (i.e. from tick to tick without a systemic infection of the host) of pathogens affects the persistence of a given disease. Using tick infestation data on roe deer, we analysed preferred attachment sites and niche width of Ixodes ticks (larvae, nymphs, males, females) and investigated the degree of inter- and intrastadial aggregation. The different development stages showed rather consistent attachment site patterns and relative narrow feeding site niches. Larvae were mostly found on the head and on the front legs of roe deer, nymphs reached highest densities on the head and highest adult densities were found on the neck of roe deer. The tick stages feeding (larvae, nymphs, females) on roe deer showed high degrees of intrastadial spatial aggregation, whereas males did not. Male ticks showed large feeding site overlap with female ticks. Feeding site overlap between larval-female and larval-nymphal ticks did occur especially during the months May–August on the head and front legs of roe deer and might allow pathogen transmission via co-feeding. Tick density, niche width and niche overlap on roe deer are mainly affected by seasonality, reflecting seasonal activity and abundance patterns of ticks. Since different tick development stages occur spatially and temporally clustered on roe deer, transmission experiments of tick-borne pathogens are urgently needed.     

Borrelia burgdorferi infection in Ixodes ricinus from habitats in Denmark

A total of 2647 ticks of the genus Ixodes was sampled by flagging the vegetation in thirty-one sites in eastern Jutland, Denmark. All ticks were identified as Ixodes ricinus Linnaeus. A total of 317 ticks (202 nymphs and 115 adults) from three different sites were examined for the spirochaete Borrelia burgdorferi Johnson et al. by indirect fluorescent antibody staining; the frequency of infection varied from 7% to 22%. It is concluded that I. ricinus, known to be the most common tick in Denmark, is the vector largely responsible for the transmission of B. burgdorferi in this country.     

Methods currently used for the control of multi-host ticks: their validity and proposals for future control strategies

Ticks have a world distribution and pest status reputation of hampering livestock production through transmission of fatal disease such as theileriosis, anaplasmosis, babesiosis, etc. and bites which cause blood loss, pain and other debilitating effects. Control of ticks is largely more effective on the host. The multi-host ticks spend most of the time off the host with short feeding periods of between four and ten days. Chemical control using dips or sprays has been the traditional method of attempting to kill these ticks during the infestation period. In many situations control, using acaricides, has been quite successful. This has been possible through correct timing of the ticks' seasonal activity and feeding periods to determine the application interval, and efficacy of the acaricides. However, the rising costs of acaricides have made it almost impossible to use these chemicals on a regular basis according to the pest problem. This is particularly true in many Third World tropical countries in which tick-associated problems are more pronounced. This has necessitated the search for alternative tick control methods on an integrated approach to pest management. For this reason, vaccination against ticks and breeding for host resistance against ticks are being studied in the hope that future control strategies will involve only the economically effective acaricide application in conjunction with these and other methods.     

Study on the infection of taiga ticks with Borrelia in the territory of Novosibirsk Scientific Center SB PAS

In our study, Borrelia were revealed in the taiga ticks Ixodes persulcatus collected on vegetation by flagging, as well as in the ticks removed from the people who asked for help in the vaccination center located in the Novosibirsk Scientific Center of the Siberian Branch of Russian Academy of Science (NS SB RAS). By the isolation of Borrelia on BSK-H medum, the occurrence of B. garinii, B. afzelii, and B. miyamotoi was established in the territory of NSC. B. miyamotoi isolates were unstable and lost their ability to growth in later passages. DNA of the same three species of Borrelia was detected by PCR in the samples of ticks, both collected on vegetation by flagging and removed from humans. DNA of B. garinii was recorded most often; DNA of B. afzelii was less frequent; and the least number of positive samples was shown for B. miyamotoi. In the ticks collected on vegetation by flagging, DNA of B. garinii was found in 38.6%, B. afzelii in 9.9%, and B. miyamoboi in 3.9% of samples. In the ticks removed from people, number of positive samples was lesser; so, DNA of B. garinii was detected in 24.2%, B. afzelii in 6.9%, and B. miyamotoi in 5.6% of samples. Mixed infection with two Borrelia species was recorded, and DNA of B. mivamnotoi more often detected simultaneously with DNA of B. garinii.