Amblyomma Limbatum Research Articles

The abundance and geographic distributions of two species of ticks in South Australia: Bundey Bore revisited

AbstractPerhaps one of the central questions in ecology has been what limits the geographic distribution of species. The geographic distributions of the reptile‐ticks Amblyomma limbatum, Bothriocroton hydrosauri and Amblyomma albolimbatum are a classic example of this problem: where these ticks meet, narrow regions‐of‐overlap often occur. Despite studies of interactions among these ticks, and of these ticks and their environment, we still do not understand what limits their geographic distributions. Many hypotheses have been proposed and tested, but all have seemingly been rejected. Our aim was to account for the abundance and the geographic distributions of A. limbatum and B. hydrosauri at Bundey Bore Station, South Australia, where these species come in contact and have been studied for over 35 years, leading to over 55 000 records of reptiles and their ticks using a capture‐mark‐recapture approach. We constructed models which had combinations of temperature and moisture indices from different months of the year to determine the relationship between climate and tick abundance, and between climate and the shifting local geographic distribution of A. limbatum and B. hydrosauri at Bundey Bore Station. We found that climate together with the abundance of ticks in the previous year and the abundance of the lizard host, accounted for 54%–77% of the variation in the abundance of A. limbatum and B. hydrosauri among years. We also found that the climate in late autumn to winter, together with the abundance of ticks and their host, accounted for 18%–84% of the variation in the geographic distributions of these ticks among years. Climate was central to the abundance and the geographic distributions of A. limbatum and B. hydrosauri at Bundey Bore Station. We speculate that the same mechanisms account for the geographic distributions of A. limbatum, B. hydrosauri and A. albolimbatum elsewhere in Australia; so, climate may explain the three‐tick problem in Austral ecology.

Amblyomma limbatum

This datasheet on Amblyomma limbatum covers Identity, Distribution, Hosts/Species Affected.

Three instances of reptile ticks parasitising humans

All ticks are haematophagous, and many exhibit some level of host specificity as adults, usually parasitizing only certain types of hosts. Amblyomma limbatum and Bothriocroton hydrosauri are generally accepted to be ectoparasites of reptiles. Herein, three instances of parasitism on humans by these ticks are reported. The observations confirm that these species will parasitize humans and provide new information about life stages and attachment sites.

Proposing a new hypothesis: Rickettsia spp. as a mechanism maintaining parapatry between two Australian reptile tick species

AbstractThis study investigates two parasitic reptile ticks — Bothriocroton hydrosauri and Amblyomma limbatum — of the sleepy lizard (Tiliqua rugosa) that abut at a 1–2 km wide parapatric boundary in South Australia. Long‐term research has investigated potential mechanisms to explain the maintenance of this boundary but has not uncovered why the distribution of A. limbatum does not extend further south. It has been previously hypothesised that pathogens may be responsible for maintaining parapatric boundaries. Rickettsia spp. has previously been reported in B. hydrosauri ticks. This study explored whether Rickettsia spp. occurs in co‐occurring A. limbatum. We observed that Rickettsia spp. was absent from all A. limbatum ticks and that 83% of examined B. hydrosauri were found to be positive with a spotted fever group Rickettsia strain. This study puts forward the hypothesis that Rickettsia spp. could contribute to the maintenance of the Mt Mary parapatric boundary between these two tick species. Further work is required to determine whether Rickettsia spp. can be transmitted from B. hydrosauri to A. limbatum and — if transmission can occur — to explore whether Rickettsia is lethal to A. limbatum ticks.

Consistent individual differences in ecto‐parasitism of a long‐lived lizard host

Individual hosts vary substantially in their parasite loads. However, whether individual hosts have consistently different loads remains uncertain. If so, hosts that have consistently high parasite loads may serve as key reservoirs or super‐spreaders. Thus, identifying whether individuals persistently differ in their parasitism and the factors that explain these patterns constitute important issues for disease ecology and management. To investigate these topics, we examined nine years of tick counts in a wild population of sleepy lizardsTiliqua rugosa. Lizards were individually marked, and throughout their activity season, often across several years, we repeatedly assessed lizards’ ticks (to stage – larva, nymph, adult male and adult female – and species, eitherBothriocroton hydrosauriorAmblyomma limbatum). Using these repeated individual measures, we determined whether tick counts were repeatable. Then, we tested predictors of average tick counts, particularly lizard mass, sex, behavioural type (aggression and boldness), and the distance between lizards’ home range centre and a road transecting the study site (an area of greater food and lizard activity). We found that lizards exhibited consistent individual differences in tick loads both within and across years. Within‐lizard yearly average counts of larvae and nymphs were positively correlated. Lizards closer to the road tended to have more larvae and nymphs of both species and more adultB. hydrosauri. Sex did not affect tick counts. Mass differentially affected adult femaleA. limbatumand adult maleB. hydrosauritick counts. Intriguingly, lizards with above average aggression but below average boldness, or vice versa, tended to have higher average adult femaleB. hydrosauritick counts. Ultimately, our results demonstrate that lizards differed consistently in their tick counts, indicating that lizard parasitism may constitute a phenotypic trait of the individual, with implications for both host–parasite dynamics and broader host ecology.

The natural history of the sleepy lizard, Tiliqua rugosa (Gray, 1825) – Insight from chance observations and long‐term research on a common Australian skink species

AbstractIn an effort to better understand the dynamics of the parapatric boundary in South Australia of the ticks Amblyomma limbatum and Bothriocroton hydrosauri the late Professor C. Michael Bull initiated studies into the ecology of sleepy lizards (Tiliqua rugosa), a common host of these parasites. These studies spanned a period of about 40 years and examined aspects such as monogamy, long‐term mate fidelity, social networks, personality, resource use and the transmission of parasites and other pathogens. This review incorporates the results of these studies with other information about this species to provide a comprehensive overview of its natural history, highlighting not only what is known, but also indicates areas that require further study.

Lizards, ticks and contributions to Australian parasitology: C. Michael Bull (1947-2016).

Professor C. Michael Bull was a great scientist and mentor, and an Associate Editor of this journal. While his research career spanned the fields of behavioural ecology, conservation biology and herpetology, in this article, we pay tribute to his major contribution to Australian parasitology. Mike authored more than eighty articles on host-parasite ecology, and revealed major insights into the biology and ecology of ticks from his long term study of the parapatric boundary of two tick species (Amblyomma limbatum and Bothriocroton hydrosauri) on the sleepy lizard (Tiliqua rugosa). In this article, we provide an overview of how this research journey developed to become one of the longest-running studies of lizards and their ticks, totalling 35 years of continuous surveys of ticks on lizards, and the insights and knowledge that he generated along that journey.

Testing the robustness of transmission network models to predict ectoparasite loads. One lizard, two ticks and four years

We investigated transmission pathways for two tick species, Bothriocroton hydrosauri and Amblyomma limbatum, among their sleepy lizard (Tiliqua rugosa) hosts in a natural population in South Australia. Our aim was to determine whether a transmission network model continued to predict parasite load patterns effectively under varying ecological conditions. Using GPS loggers we identified the refuge sites used by each lizard on each day. We estimated infectious time windows for ticks that detached from a lizard in a refuge. Time windows were from the time when a detached tick molted and become infective, until the time it died from desiccation while waiting for a new host. Previous research has shown that A. limbatum molts earlier and survives longer than B. hydrosauri. We developed two transmission network models based on these differences in infective time windows for the two tick species. Directed edges were generated in the network if one lizard used a refuge that had previously been used by another lizard within the infectious time window. We used those models to generate values of network node in-strength for each lizard, a measure of how strongly connected an individual is to other lizards in the transmission network, and a prediction of infection risk for each host. The consistent correlations over time between B. hydrosauri infection intensity and network derived infection risk suggest that network models can be robust to environmental variation among years. However, the contrasting lack of consistent correlation in A. limbatum suggests that the utility of the same network models may depend on the specific biology of a parasite species.

Coxiella burnetii in Western Barred Bandicoots (Perameles bougainville) from Bernier and Dorre Islands in Western Australia

The aim of this work is to investigate the presence of Coxiella burnetii in Perameles bougainville and their ticks on two islands off Western Australia. Haemaphysalis humerosa, Haemaphysalis ratti, and Haemaphysalis lagostrophi were collected from P. bougainville on Bernier and Dorre Islands from 2005 to 2007; only Amblyomma limbatum was collected from humans over the same interval. One of 13 tick samples and 1 of 12 P. bougainville fecal samples were positive for C. burnetii DNA using quantitative polymerase chain reaction. DNA fragments had >99% similarity to published C. burnetii sequences. Three of 35 P. bougainville sera tested positive for anti-C. burnetii antibodies using enzyme-linked immunosorbent assay. C. burnetii was found in P. bougainville feces and a H. humerosa tick on Dorre Island and Bernier Island, respectively. This is the first reported use of enzyme-linked immunosorbent assay for screening of P. bougainville sera. The risk of zoonotic Q fever infection for human visitors to these islands is considered relatively low, however, appropriate precautions should be taken when handling western barred bandicoots, their feces and their ticks on Bernier and Dorre Islands.

Refuge sharing network predicts ectoparasite load in a lizard

Living in social groups facilitates cross-infection by parasites. However, empirical studies on indirect transmission within wildlife populations are scarce. We investigated whether asynchronous overnight refuge sharing among neighboring sleepy lizards, Tiliqua rugosa, facilitates indirect transmission of its ectoparasitic tick, Amblyomma limbatum. We fitted 18 neighboring lizards with GPS recorders, observed their overnight refuge use each night over 3 months, and counted their ticks every fortnight. We constructed a transmission network to estimate the cross-infection risk based on asynchronous refuge sharing frequencies among all lizards and the life history traits of the tick. Although self-infection was possible, the network provided a powerful predictor of measured tick loads. Highly connected lizards that frequently used their neighbors’ refuges were characterized by higher tick loads. Thus, indirect contact had a major influence on transmission pathways and parasite loads. Furthermore, lizards that used many different refuges had lower cross- and self-infection risks and lower tick loads than individuals that used relatively fewer refuges. Increasing the number of refuges used by a lizard may be an important defense mechanism against ectoparasite transmission in this species. Our study provides important empirical data to further understand how indirectly transmitted parasites move through host populations and influence individual parasite loads.

Unique biological rhythm in the reproductive behaviour of female ticks of reptiles

We report the discovery of a biological rhythm in the reproductive behaviour of the tick Bothriocroton hydrosauri that was absent in Amblyomma limbatum, a species that occurs on the same species of reptile host. Female B. hydrosauri mated in autumn or winter delayed oviposition until the following spring, while there was no diapause in conspecific females mated in spring or early summer. Initiation of ovipositional diapause in ticks is usually related to photoperiodic stimuli, but this was not the case for B. hydrosauri. The sinusoidal pattern in pre-oviposition times of B. hydrosauri females mated in different months in the laboratory suggests an internal seasonal time-keeping mechanism. We hypothesize that hormones imbibed by females during their bloodmeal may provide environmental cues associated with the induction of diapause. Irrespective of the mechanism underlying the rhythm, diapause by B. hydrosauri females mated during autumn or winter is of adaptive advantage because it synchronizes oviposition with favourable environmental conditions for egg hatching and increases the chance of larvae finding a host. The lack of a similar biological rhythm in A. limbatum may be a reflection of the different environmental conditions this species experiences throughout most of its range as compared with B. hydrosauri.

The distribution of reptile ticks in South Australia: more complex than assumed

An isolated population of a reptile tick closely resembling Amblyomma limbatum is reported from a very small area of saltpan vegetation near Lochiel in South Australia. This population lies well outside the known range of A. limbatum, and most specimens are distinguished from this species by a small second ridge or spur on coxa II. The discovery of this pocket suggests that the distribution of reptile ticks in Australia may be more complex than previously assumed.

Interactions between climate, host refuge use, and tick population dynamics

The relationship between Australian sleepy lizard (Tiliqua rugosa) microhabitat use and tick (Amblyomma limbatum) population dynamics was investigated. Over 3 years (2002-2004) between 23 and 50 lizards were radio-tracked up to four times a week to record microhabitat use and each fortnight to determine tick loads. Daily maximum temperature was highly predictive of lizard microhabitat use. In hotter fortnights lizards used larger bushes and burrows for refuge. Peak background tick infestation levels and pulses of attachment coincided with higher ambient temperature. Male ticks attached throughout the year independent of season. Engorged females detached late in spring, summer and autumn, when climate regularly restricted lizards to a few thermally conservative refuges. Peak nymph and larval attachment occurred over summer and into autumn. Climate-dependent timing and type of host refuge use may influence tick population density. In more temperate summers lizards may avoid refuges with potentially high parasite loads.

Ultrastructure of developmental stages of Hemolivia mariae (Apicomplexa: Haemogregarinidae), natural parasite of the Australian sleepy lizard, in experimentally infected deviant hosts.

Mabuya vitatta (Olivier) (Scincidae) and Agama stellio (L.) (Agamidae) were infected with Hemolivia mariae Smallridge et Paperna, 1997 by ingestion of tick viscera from Amblyomma limbatum Neumann, fed as nymphs on naturally infected Australian sleepy lizards, Tiliqua rugosa Gray. The unnatural infection apparently interfered with the developmental schedule of the parasites. Transmission electron microscopic images of merogonic stages were obtained, as well as images of early developing gametocytes. Tissue and intraerythrocytic meronts were bound by a hardened wall. Intraerythrocytic gametocytes were lodged in a parasitophorous vacuole, which was filled with granular material, and were bound by a two-membrane wall. Small and large osmiophilic bodies were located in a sub-pellicular position. With differentiation, the wall membranes tightened with the parasitophorous vacuole wall, and the osmiophilic bodies disappeared. The outer parasite membrane consolidated into a thick encasing with distinct sutures. Late infection in A. stellio comprised gametocytes only.

Temporal and spatial dynamics of a parapatric boundary between two Australian reptile ticks

Two tick species Aponomma hydrosauri and Amblyomma limbatum that infest large reptiles have an abrupt parapatric boundary near Mt Mary in South Australia. A previous model has suggested that the boundary is maintained at population density troughs resulting from habitat heterogeneity along a gradual environmental gradient. This paper describes the dynamics of the boundary on three transects over 17 years, 1982-98. Over the last seven years of that period there has been a significant increase in rainfall. At the same time, the boundary position has moved 1-2 km on the transects, with the more mesic adapted Ap. hydrosauri advancing into the distribution of the more xeric adapted Amb. limbatum. Also over the same time the density of ticks on lizards in regions flanking the boundary zone has increased for Ap. hydrosauri and decreased for Amb. limbatum. These results suggest that the environmental gradient has been altered, perhaps by increased rainfall, to favour Ap. hydrosauri, which has been able to colonize more successfully across the density troughs and extend its distribution.

Prevalence of infection by the protozoan Hemolivia mariae in ticks.

This paper considers the prevalence of natural infections of the protozoan Hemolivia mariae, in its hosts the Australian sleepy lizard, Tiliqua rugosa, and the ixodid tick species, Amblyomma limbatum. We investigate whether the protozoan may be influencing the tick population in the field, by comparing the observed prevalence of infection in ticks with the prevalence expected from known transmission dynamics. The prevalence of infection in nymphs was similar to the expected prevalence, but the observed prevalence in adults was higher than expected. These results provide no evidence for infection-induced mortality in ticks. We also found that tick loads on infected and uninfected lizards were not significantly different and, overall, infected lizards were as likely to be tick-infested as uninfected lizards. However, infected lizards were less likely to be found carrying female ticks. On balance, the evidence did not strongly support the hypothesis that ticks avoid feeding on infected lizards. We use known parameters of H. mariae transmission to estimate the rate of tick ingestion that may be required to sustain the observed prevalences in the field.

Influence of temperature and relative humidity on the moulting success of Amblyomma limbatum and Aponomma hydrosauri (Acari: Ixodidae) larvae and nymphs

This study compared the duration of the moulting periods of engorged larvae and nymphs of the ixodid ticks, Amblyomma limbatum and Aponomma hydrosauri, at different temperature/relative humidity regimes, and examined the relationships between the engorged weight of ticks and their weights after moulting. The results showed that for each species, there was a significant relationship between the weights of unfed nymphs and engorged larvae, and the weights of unfed adults and engorged nymphs. The weight of engorged nymphs was also a good indicator of their sex, with female ticks having heavier weights as engorged nymphs. Temperature and relative humidity had a marked effect on the moulting success of engorged ticks of both species. Aponomma hydrosauri larvae and nymphs were able to moult at lower temperatures than Amb. limbatum but most ticks, except Ap. hydrosauri larvae, failed to moult at 13°C. Additionally, there was a marked decrease in the pre-moult times of ticks at higher temperatures, with larvae taking less time to moult than nymphs. At temperatures greater than 21°C, Amb. limbatum took less time to moult than Ap. hydrosauri but this interspecific difference was less marked for nymphs. The interspecific differences in the responses of engorged larvae and nymphs to different temperatures and relative humidities correlated with interspecific differences in off-host behaviour and with the different climates the two species experience throughout most of their distributional range.

Prevalence and intensity of the blood parasite Hemolivia mariae in a field population of the skink Tiliqua rugosa.

The impacts of virulent parasites on humans or domestic animals are well documented. Less is known of the impact of parasites in natural host-parasite associations. A population of the Australian sleepy lizard Tiliqua rugosa is infected with the blood microparasite Hemolivia mariae, which is transmitted by the ectoparasitic tick Amblyomma limbatum. In most infected lizards a very small proportion, usually < 1%, of red blood cells are infected. A study of the prevalence of the microparasite in the field population found no difference either over 5 years of study or among times within a lizard activity season. Juvenile and sub-adult lizards and larger adults were less frequently infected with H. mariae than were other adults. In sub-adults this was related to a lower level of tick infestation. In adults, male and female lizards were equally frequently infected with H. mariae, but the presence or absence of ticks was not predictive of infection. The lizards' body condition was measured as the residual of the regression of log snout-vent length against log body mass. In female lizards the body condition was not affected by infection. In males the body condition declined over the sampling period each year, probably as a result of mate attendance. The body condition was poorer in male lizards with H. mariae infection than in uninfected males. Possible explanations for the associations of microparasites and host lizards are discussed.

Ultrastructure of Hemolivia mariae gamonts in the blood of the lizard Tiliqua rugosa and their development to oocyst stage in the tick Amblyomma limbatum

The ultrastructural features of the development of Hemolivia mariae from intra-erythrocytic gamonts in their host, the Australian lizard Tiliqua rugosa, to oocysts containing sporokinetes in their vector, the tick Amblyomma limbatum, are described. Mature intra-erythrocytic gamonts, as well as gamonts ingested by the tick were encased in a thick (30 nm) capsule with distinct suture sites at each of the two apices. In the only image of a presumed syzygy, both partners were still encased. Further stages, the young and ongrowing oocysts, were bound by a membranous wall. Sporokinetes developed within the oocyst around a primordial crystalloid body. The fully differentiated sporokinetes, still resting within the oocyst wall, exhibited a very short conoid in the apical complex and were heavily loaded with crystalloid material.

Ultrastructure studies on post-oocyst development of the lizard hemogregarine Hemolivia mariae in the tick Amblyomma limbatum.

The ultrastructural features of the development of Hemolivia mariae, a blood parasite of the Australian lizard, Tiliqua rugosa, from sporokinetes to sporozoites in their vector tick Amblyomma limbatum are described. Sporokinetes, released from oocysts, re-establish themselves in tick-gut epithelial cells within a parasitophorous vacuole, the wall of which becomes evaginating and anastomosing and is underlined extensively by endoplasmic reticulum. The sporozoites forming within the encysting sporokinete body become bordered by a prominent thick wall, which eventually forms the resistant sporocyst wall. The main differences between the ultrastructural features of Hemolivia and those of other hemogregarine taxa are discussed.