Population dynamics and density-dependent seasonal mortality indices of the tick Rhipicephalus appendiculatus in eastern and southern Africa

Abstract. Eight sets of previously published data on the seasonal abundance of the tick Rhipicephalus appendiculatus in Burundi, Uganda, Tanzania and Zimbabwe are analysed to yield seasonal mortality indices. Correlations between these indices and abiotic (climatic) and biotic (tick density) variables suggest that it is the stage from females to larvae that is most sensitive to adverse abiotic conditions, specifically low moisture availability. Mortality at the other stages of the tick's life cycle is strongly density-dependent. The precise nature of this density-dependence suggests that it may be caused by acquired resistance to ticks by cattle. Robust correlations between satellite-derived vegetation indices, climatic factors and mortality indices suggest that detailed climatic data, often unavailable, may be replaced by satellite data, now widely available, for use in modelling tick populations.     

The effect of rainfall on tick challenge at Kyle Recreational Park,Zimbabwe

The effect of rainfall pattern on tick challenge was investigated at Kyle Recreational Park, Zimbabwe, from 1991 to 1992 using drag and removal plot methods to sample environmental tick density. The abundance of adults and nymphs of the brown ear-tick Rhipicephalus appendiculatus and larvae of the bont tick Amblyomma hebraeum was positively correlated with monthly rainfall, whereas no relationship with rainfall was revealed for larval R. appendiculatus, adults of the red-legged tick R. evertsi, or larvae of the blue tick Boophilus decoloratus. A comparison between 1991 (490 mm rainfall) and the drought year of 1992 (161 mm) revealed significant differences in the abundance of R. appendiculatus, A. hebraeum, and B. decoloratus. During the wet season, R. appendiculatus adults were 2–3 time more numerous in the environment during the higher rainfall year of 1991. A. hebraeum larval abundance exhibited a similar pattern to that of R. appendiculatus adults, but B. decoloratus larvae were more abundant in the drought year of 1992 during both the wet and dry seasons. Comparable tick abundance data collected at Kyle during the above-average rainfall years of 1975–1977 (mean = 1029 mm) were compared with tick challenge during the below-average rainfall years of 1991–1992 (mean = 326 mm). In grassland sand habitat and all habitats combined R. appendiculatus adults, nymphs, and larvae were much more abundant during the high rainfall years. In contrast, larvae of B. decoloratus were more numerous during the drier years. A. hebraeum larvae were also more abundant during the drier years. The strong positive correlation of adult R. appendiculatus abundance with rainfall and the coincidence of increased adult tick challenge with increased rainfall indicates that adult R. appendiculatus tick burden on hosts would be heaviest during the wet season and high rainfall years.     

Monitoring of naturally acquired and artificially induced immunity toAmblyomma variegatum andRhipicephalus appendiculatus ticks under field and laboratory conditions

The ability of rabbits, goats and cattle to acquire immunity to the ixodid ticksAmblyomma variegatum andRhipicephalus appendiculatus was studied under laboratory and field conditions. Rabbits were successfully immunized with crude salivary gland extract (SGE) and midgut extract (ME) obtained from flat or partly fed femaleR. appendiculatus ticks. The lowest numbers of larvae were produced by females fed on rabbits immunized with unfed midgut extract. Similar reductions in larval production could be induced after three infestations of rabbits with adultR. appendiculatus. Also, successive feedings of nymphs ofR. appendiculatus on rabbits resulted in significantly reduced engorgement weights. Skin testing with SGE induced delayed-type hypersensitivity reactions, which could be correlated with immunity toR. appendiculatus in rabbits. Moreover, circulating antibodies were detected in rabbits with an ELISA using SGE ofR. appendiculatus.Immunity toA. variegatum nymphs could be induced in rabbits by repeated infestations, but this failed in goats. Immunization of goats with midgut extract from adultA. variegatum did not protect against subsequent nymphal challenge, but strong skin reactions were noticed when adults ticks fed on immunized goats. Sodium dodecyl sulfate polyacrylamide gel electrophoresis of SGE and ME fromA. variegatum revealed the presence of 48 protein bands in SGE and 29 bands in midgut extract. Western blotting employing serum from a rabbit immune toR. appendiculatus recognized a number of bands in SGE fromR. appendiculatus, but also in SGE ofA. variegatum.Immunity acquired by cattle to ixodid tick infestations under field conditions was monitored by skin testing with SGE and western blot analysis. In general, cattle with the lowest tick numbers manifested the strongest delayed-type hypersensitivity responses. Finally, western blot analysis employing sera from tick-infested and tick-naive cattle could not be related to actual immune status.     

An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus

The wide geographic and climatic range of the tick Ixodes ricinus, and the consequent marked variation in its seasonal population dynamics, have a direct impact on the transmission dynamics of the many pathogens vectored by this tick species. We use long-term observations on the seasonal abundance and fat contents (a marker of physiological ageing) of ticks, and contemporaneous microclimate at three field sites in the UK, to establish a simple quantitative framework for the phenology (i.e. seasonal cycle of development) of I. ricinus as a foundation for a generic population model. An hour-degree tick inter-stadial development model, driven by soil temperature and including diapause, predicts the recruitment (i.e. emergence from the previous stage) of a single cohort of each stage of ticks each year in the autumn. The timing of predicted emergence coincides exactly with the new appearance of high-fat nymphs and adults in the autumn. Thereafter, fat contents declined steadily until unfed ticks with very low energy reserves disappeared from the questing population within about 1 year from their recruitment. Very few newly emerged ticks were counted on the vegetation in the autumn, but they appeared in increasing numbers through the following spring. Larger ticks became active and subsequently left the questing population before smaller ones. Questing tick population dynamics are determined by seasonal patterns of tick behaviour, host-contact rates and mortality rates, superimposed on a basal phenology that is much less complex than has hitherto been portrayed.     

Comparative off‐host survival of larval Rocky Mountain Wood Ticks (Dermacentor andersoni) collected from ecologically distinct field populations

Dermacentor andersoni (Ixodida: Ixodidae) Stiles, also known as the Rocky Mountain Wood Tick (RMWT), is found throughout the western United States and transmits pathogens of importance to human and animal health. The distributions and activity patterns of RMWTs are shaped by regional climatic variation. However, it is unknown if responses to climatic variation differ across the tick's geographical range. The objective of this narrow study was to test the hypothesis that the responses of RMWTs to abiotic conditions [e.g. temperature and RH (relative humidity)] vary among populations. We collected RMWTs from ecologically distinct field sites in the states of Montana and Oregon (USA). In the laboratory, we tracked weekly survival of tick larvae under four combinations of RH (75% and 98%) and temperature (26 and 32 °C) that reflected the range of conditions observed in the source habitats during spring‐summer. For both populations, larval survival time decreased at the higher ambient temperature (50% mortality 1–2 weeks earlier). Differences in RH did not affect the survival time of larvae from Oregon. By contrast, the survival time of larvae from Montana decreased at the lower RH (50% mortality 1 week earlier). These data suggest that the tolerance limits for water stress may differ among populations of D. andersoni.     

Deconstructing Ixodes ricinus: a partial matrix model allowing mapping of tick development,mortality and activity rates

A stage‐structured Leslie matrix model of a partial, discrete population of Ixodes ricinus (Linnaeus) (Ixodida: Ixodidae) ticks was developed to elucidate the impact of climate trends on the distribution and phenology of this species in the western Palaearctic. The model calculates development and mortality rates for each instar and evaluates recruitment rates based on the development of the tick population. The model captures the changes in development and mortality rates, providing a coherent index of performance correlated with the tick's geographic range. Maximum development rates are recorded for latitudes south of 36 °N and are spatially correlated with sites of maximum temperature, highest saturation deficit and highest mortality. The maximum available developmental time (the total annual time during which temperature allows development) for I. ricinus in the western Palaearctic is < 45% of the total year. North of 60 °N, available developmental time decreases sharply to only 15% of the year. The latitudinal boundary at which survival rates sharply drop is 43–46 °N, clearly delimiting the classically recognized extent of the main tick populations. The pattern of activity for larval–nymphal synchrony shows a clear west–east pattern. The model demonstrates the impact of climate according to tick stage and geographic location, and provides a practical framework for testing how the tick's lifecycle is affected by climate change.     

Towards an Evolutionary Understanding of Questing Behaviour in the Tick Ixodes ricinus

The tick Ixodes ricinus finds its hosts by climbing vegetation and adopting a sit-and-wait tactic. This “questing” behaviour is known to be temperature-dependent, such that questing increases with temperature up to a point where the vapor pressure deficit (drying effect) forces ticks down to rehydrate in the soil or mat layer. Little if any attention has been paid to understanding the questing of ticks from an evolutionary perspective. Here we ask whether populations from colder climatic conditions respond differently in terms of the threshold temperature for questing and the rate of response to a fixed temperature. We find significant variation between populations in the temperature sensitivity of questing, with populations from cooler climates starting questing at lower temperatures than populations from warmer temperatures. Cool climate populations also quest sooner when the temperature is held constant. These patterns are consistent with local adaptation to temperature either through direct selection or acclimation and challenge the use of fixed thresholds for questing in modeling the spread of tick populations. Our results also show how both time and temperature play a role in questing, but we are unable to explain the relationship in terms of degree-time used to model Arthropod development. We find that questing in response to temperature fits well with a quantitative genetic model of the conditional strategy, which reveals how selection on questing may operate and hence may be of value in understanding the evolutionary ecology of questing.     

High-resolution predictive mapping for Rhipicephalus appendiculatus (Acari: Ixodidae) in the Horn of Africa

The brown ear tick Rhipicephalus appendiculatus, vector of East Coast fever (ECF) and related cattle diseases caused by Theileria parva has never been reported from the Horn of Africa. Habitat suitability for this tick species was predicted using Maxent modelling technique based on R. appendiculatus records in Sub-Saharan Africa. Two models were developed: the first is based on the tropical R. appendiculatus distribution and the one is based on the distribution records in the temperate region of Sub-Saharan Africa. The tropical model shows favourable habitat in much of the Ethiopian highlands. The whole Djibouti, the south eastern Ethiopian lowlands, majority of Somalia and Eritrea were found to be not suitable for the survival and development of this tick species. Highly suitable areas occur in areas which have moderate temperature and high precipitation. Introductions of R. appendiculatus into the Horn of Africa probably have been prevented by the natural barrier between the known R. appendiculatus distribution range in East Africa and the Horn of Africa. The effect of an introduction of R. appendiculatus and thereby ECF into the Horn of Africa could be catastrophic since the cattle in this area have no immunity against ECF, and mortality might be considerable in all age groups of cattle.     

The life cycle of Ixodes rubicundus (Acari: Ixodidae) and its adaptation to a hot,dry environment

The life cycle of Ixodes rubicundus, the Karoo paralysis tick, was studied under field conditions in the south-western Orange Free State, South Africa, by placing freshly engorged ticks in small containers. The life cycle extends over 2 years. The two regulating phases in the life cycle, which undergo a morphogenetic diapause during the hot and dry summer months, are the egg and engorged nymph. Possible behavioural diapause in adults which suppresses questing activity before the end of March. can also serve as a third regulating phase. Temperature affects the duration of the pre-oviposition period of engorged females and the period between detachment of engorged larvae from hosts and ecdysis. Commencement of larval hatch is reasonably synchronized, irrespective of the month during which oviposition occurred. Peak activity periods of larvae (April or May) occur during a period of high rainfall and decreasing daily maximum temperatures. The period between detachment of engorged nymphs from hosts and ecdysis is highly variable (8–36 weeks). All developmental stages of the tick occur mainly during autumn and winter and no ticks are active during the hot summer months of December to February. Larvae, nymphs and adults each survive for only one season.     

In-vivo effects of ivermection onRhipicephalus appendiculatus: the influence of tick feeding patterns and drug pharmacokinetics

Sublethal effects seen amongstRhipicephalus appendiculatus feeding on ivermectin-treated rabbits were diverse and dependent both on drug dose, pharmacokinetics and tick feeding patterns: changes in drug formulation, the time of infestation relative to treatment, and the tick instar used, profoundly influenced acaricidal activity. Death was a sequel to paralysis only if tick feeding was interrupted for sufficient time to produce irreversible dehydration. Concurrent pharmacokinetic investigations revealed that, for the larvae ofR. appendiculatus, the mean critical lethal dose of ivermectin imbibed over a 5-day engorgement period was 3500 g/kg. This quantity of ivermectin was achieved in the blood-meals of larvae feeding on rabbits treated subcutaneously with a single dose of Ivomec injection (MSD)^*800 g/kg, provided infestation took place within 24 h of treatment. At lower drug doses, or if larval infestations were delayed for>24 h post-treatment, the quantity of circulating ivermectin (and thus imbibed by the tick larvae) fell below 3500 g/kg and an increasing percentage of larvae successfully engorged and detached. More than 90% of such larvae moulted to the nymphal stage. Nymphae and larvae exhibited similar susceptibility to ivermectin on treated rabbits which could be explained by similar feeding patterns. However, adult female and male ticks were markedly less susceptible and interpretation of ivermectin-induced effects was more complex.     

Acquired resistance to ixodid ticks induced by tick cement antigen

Antisera from guinea pigs made resistant to infestation with an ixodid tick of east and central Africa,Rhipicephalus appendiculatus, were used to identify the tick antigens they recognized by immunoblotting. Most of the antigens were found in tick salivary glands and in tick attachment cement. Antisera fromR. appendiculatus-resistant guinea pigs also recognized some salivarygland antigens in ticks of other species (R. pulchellus, R. evertsi, Amblyomma variegatum andA. gemma). Antibodies against the most strongly recognizedR. appendiculatus antigen, a 20-kDa molecule, were only poorly reactive with similar-sized molecules in the other ticks. A 94-kDa antigen, which appeared to have broader cross-reactivity, was purified fromR. appendiculatus attachment cement, and a monospecific rabbit serum was raised against it. This antiserum clearly recognized a molecule of similar molecular weight inR. pulchellus andR. evertsi. Intravenous inoculation of rabbits with the purified molecule elicited delayed-type hypersensitivity to the antigen. The hypersensitive rabbits demonstrated resistance to feeding ofR. appendiculatus ticks but slight enhanced feeding ofR. pulchellus ticks. These results are discussed with respect to their relevance for artificial induction of tick-feeding resistance.     

Diel activity of Ixodes ricinus Acari: Ixodidae at two locations near Stockholm, Sweden

The diel ‘activity’, i.e. availability, of Ixodes ricinus larvae, nymphs and adults was investigated in a meadow and a forest habitat near Stockholm during 1991–1993. Generally, the immature ticks were more prevalent in the forest than in the meadow. In the meadow, the mean larval and adult numbers varied significantly between 4 h time intervals with the peak activity from 2300 to 0300 h. In the forest, the tick numbers did not differ significantly between the time intervals. The association of the tick activity with certain meteorological variables was strongest in the meadow, where the mean numbers of all tick stages were negatively correlated with the temperature. The relative humidity was positively correlated only with the mean numbers of larvae. In contrast, the larval activity in the forest was positively and negatively correlated with the temperature and relative humidity, respectively, while the nymphal and adult activity showed no association with these climatic variables. The impact of the host activity on the tick diel activity is also discussed.     

Artificial-membrane feeding of the ixodid tick,Rhipicephalus appendiculatus,to repletion

An artificial feeding device was constructed with a Baudruche, membrane bearing olfactory and tactile stimuli, to induce voluntary attachment and feeding of the brown ear tick,Rhipicephalus appendiculatus. Preparation of the membrane and experimental conditions used are described. Unfed adults ofR. appendiculatus, 2–3 weeks after moulting, were confined on the membrane, which was treated with cattle ear-wash and other stimuli. They attached and commenced sucking blood within 12–48 h. Fully engorged ticks started detaching from the membrane on the 6th day. After a 5–6-day incubation period, they started laying eggs which hatched into normal larvae.     

Influence of selected meteorological variables on the questing activity of Ixodes ricinus ticks in Lower Silesia,SW Poland

The relationship between climate data and tick questing activity is crucial for estimation of the spatial and temporal distribution of the risk of ticks and tick‐borne diseases. This study establishes correlations between selected meteorological variables provided by the Weather Research and Forecasting model (WRF) and the questing activity of Ixodes ricinus nymphs and adults on a regional scale across Lower Silesia, Poland. Application of Generalized Linear Mixed Models (GLMM), built separately for adults and nymphs, showed that solar radiation, air temperature, and saturation deficit appeared to be the meteorological variables of prime importance, whereas the wind speed was less important. However, the effect of meteorological parameters was different for adults and nymphs. The adults are also more influenced by forest cover and the percentage of forest type if compared to nymphs. The WRF model providing meteorological variables separately for each location and day of tick sampling can be useful in studies of questing activity of ticks on a regional scale.     

Densities of Ixodes ricinus ticks (Acari: Ixodidae) on moorland vegetation communities in the UK

Unfed (questing) Ixodes ricinus ticks were collected by blanket dragging on a monthly basis from heather-dominated, Vaccinium-dominated and bracken-dominated vegetation communities from two different biogeographical regions of the UK (the Quantock Hills in Somerset, south west England and the North York Moors, north east England) throughout the spring and summer months of 1991 and 1992. Eighteen sites were monitored across the two regions and a total of 1920 blanket drags were carried out. Vaccinium sites showed high tick densities at all life stages, as did bracken sites. Significantly lower numbers of larval and nymphal ticks per drag were collected on heather sites than were collected on either Vaccinium (bilberry/whortleberry) or bracken sites, while similar numbers of adult ticks per drag were collected from each of the three vegetation communities. There was no significant difference between the mean numbers of any tick life stage collected on the Quantock Hills and those collected on the North York Moors on these vegetation communities or between the mean numbers of any tick life stage collected in 1991 and those collected in 1992 on these vegetation communities.     

Introduced Siberian chipmunks are more heavily infested by ixodid ticks than are native bank voles in a suburban forest in France

By serving as hosts for native vectors, introduced species can surpass native hosts in their role as major reservoirs of local pathogens. During a 4-year longitudinal study, we investigated factors that affected infestation by ixodid ticks on both introduced Siberian chipmunks Tamias sibiricus barberi and native bank voles Myodes glareolus in a suburban forest (Forêt de Sénart, Ile-de-France). Ticks were counted on adult bank voles and on adult and young chipmunks using regular monthly trapping sessions, and questing ticks were quantified by dragging. At the summer peak of questing Ixodes ricinus availability, the average tick load was 27-69 times greater on adult chipmunks than on adult voles, while average biomass per hectare of chipmunks and voles were similar. In adult chipmunks, individual effects significantly explained 31% and 24% of the total variance of tick larvae and nymph burdens, respectively. Male adult chipmunks harboured significantly more larvae and nymphs than adult females, and than juveniles born in spring and in summer. The higher tick loads, and more specifically the ratio of nymphs over larvae, observed in chipmunks may be caused by a higher predisposition - both in terms of susceptibility and exposure - to questing ticks. Tick burdens were also related to habitat and seasonal variation in age- and sex-related space use by both rodents. Introduced chipmunks may thus have an important role in the dynamics of local vector-borne pathogens compared with native reservoir hosts such as bank voles.     

Woodland biodiversity management as a tool for reducing human exposure to Ixodes ricinus ticks: A preliminary study in an English woodland

This paper presents preliminary findings towards developing a UK‐specific approach to reducing public exposure to woodland questing Ixodes ricinus tick populations by harnessing existing biodiversity‐enhancing woodland ride (i.e., linear non‐wooded herbaceous habitat either side of track within woodland) management strategies. This preliminary study in an English woodland firstly assesses whether ecological and environmental factors determine presence and density of questing Ixodes ricinus along woodland rides. Secondly, it sets these findings in the context of woodland ride management guidelines in England in order to understand what impact ride management strategies might have on numbers of questing ticks and tick survival. Nymph and adult I. ricinus presence and abundance were modelled in relation to relevant microclimate and ecological parameter variables. Predictor variables for increased questing nymph abundance included ride orientation, mat depth, occurrence of bracken/bramble and animal tracks, ride/path width, and sward height. Ticks thrive in the ecotonal habitat of a woodland ride, therefore we urge woodland managers to consider the impact of their ride management on ticks and human exposure to ticks. Possible recommendations for mitigating questing I. ricinus in line with biodiversity management guidelines rides are discussed in this paper and include seasonal mowing regimes, management of mulch/mat, and bracken/bramble management through use of scalloped ride edges.     

Introduction,spread and subsequent disappearance of the brown ear-tick,Rhipicephalus appendiculatus,from the southern lowveld of Zimbabwe

According to the climate-matching model CLIMEX the hot, dry lowveld of Zimbabwe is unsuitable for the survival of the brown ear-tickRhipicephalus appendiculatus. There is evidence that the tick was absent from the lowveld in the 1960s but was introduced in 1973 and spread over a large area before disappearing in 1983. It was introduced at the start of a wet cycle when, according to CLIMEX predictions, conditions were suitable for its survival, and it disappeared at the end of a dry cycle when conditions were unsuitable. The most important factor in the disappearance of the tick appeared to be heat stress. The study has provided an illustration of the dynamic distribution ofR. appendiculatus and field validation of the CLIMEX model.     

Repellent and acaricidal properties of Ocimum suave against Rhipicephalus appendiculatus ticks

An oil extracted from the leaves of a tropical shrub Ocimum suave was found to repel as well as kill all stages of the tick Rhipicephalus appendiculatus. In an in vitro bioassay for the larvae, the LC₅₀ of the oil in liquid paraffin was 0.024%. A 10% solution was found to kill all immatures and more than 70% of adults feeding on rabbits. Rabbits were protected for 5 days against attaching larvae using a 10% solution. Preliminary experiments undertaken with cattle kept in the field suggest that the oil may have potential in tick control, and a role in integrated tick management.     

Climate impacts on blacklegged tick host-seeking behavior

The nymph of the blacklegged tick (Ixodes scapularis), the primary North American vector of the causative agent of Lyme disease, must attach to a host by the end of its questing season in order to feed and subsequently molt into an adult. The proper timing of this behavior is critical both for the tick’s survival and for perpetuating the transmission of tick-borne pathogens. Questing also depletes limited nymphal lipid reserves and increases desiccation risk. Given this tradeoff, questing behavior and its environmental influences can be expressed in a dynamic state variable model. We develop what we believe to be the first such model for a tick, and investigate the influence of climate on nymph fitness predictions. We apply these results to the hypothesized inland migration of I. scapularis from island refugia, evaluating fitness under suboptimal questing strategies and uncertain environmental conditions.