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

This 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.     

Competition for sites of attachment to hosts in three parapatric species of reptile tick

Summary Competition for sites of attachment to hosts by three species of reptile tick, Aponomma hydrosauri, Amblyomma albolimbatum and Amb. limbatum was investigated as a possible cause for the parapatric distributions found in these species throughout southern Australia. Two localities were chosen for detailed study; a boundary between Ap. hydrosauri and Amb. limbatum near Mt. Mary in the mid-north of South Australia and a boundary between Ap. hydrosauri and Amb. albolimbatum near Arno Bay on the Eyre Peninsula of South Australia. Comparisons of sites of attachment to hosts were made between hosts infested by one species of tick and hosts infested by two species of tick. At Mt. Mary, Ap. hydrosauri and Amb. limbatum adults attach more commonly in the ears and on the midback of their hosts, however, no evidence was found to suggest that competition between the species occurred for these sites. At Arno Bay, Amb. albolimbatum adults had similar sites of attachment to hosts as the other two species, however, significantly more of this species attach in the ears of their hosts. There is no difference in sites of attachment to hosts of Ap. hydrosauri females at Arno Bay and Mt. Mary. Ap. hydrosauri males at Arno Bay, however, show a shift in sites of attachment to hosts away from those sites occupied by Amb. albolimbatum males and females. This shift occurs only in cases where Amb. albolimbatum did not infest the same host. Although the shift in male Ap. hydrosauri sites of attachment to hosts can be explained in terms of past competition, there is no evidence to suggest that such competition in the past, or competition at present, maintains the parapatric boundaries found in these species of thick.     

Niche changes between parasite populations: An example from ticks on reptiles

Summary Two Australian tick species Aponomma hydrosauri and Amblyomma albolimbatum have the same major host species, the lizard Trachydosaurus rugosus. While females of Amb. albolimbatum are most often attached in the ears and on the neck of their hosts, Ap. hydrosauri females prefer to attach further back, under the forearms and on the back. Males show the same interspecific difference but there is also a difference between populations. Ap. hydrosauri males from populations in contact with Amb. albolimbatum attach more often in posterior positions than Ap. hydrosauri males from populations isolated from Amb. albolimbatum. These differences were found in both field populations and laboratory reared ticks. Phylogenetic evidence suggests that the change in male attachment site between Ap. hydrosauri populations followed the colonization of T. rugosus. We propose that the most likely reason for the change of attachment sites has been interspecific interactions with Amb. albolimbatum and that competition has been for space for efficient reception of female signals.     

Laboratory studies of ant predation on parapatric reptile ticks

Abstract Two reptile tick species, Aponomma hydrosauri and Amblyomma limbatum, have a parapatric distribution in South Australia. Predation may play a role in maintaining the boundary. Laboratory colonies of Rhytidoponera and Iridomyrmex ants were collected from near Mt Mary, South Australia, close to the tick boundary. They were tested as predators of the two tick species. In the experiments, ticks in leaf litter were more protected from predation than those on bare soil. When comparing leaf litter types from the Mt Mary area, mallee litter was more protective than bluebush litter of equivalent depth. Ticks positioned at the base of the litter layer were more protected from predation than those at the litter surface, and Amb. limbatum ticks were more resistant to predation than Ap. hydrosauri ticks. These results contribute to our understanding of the mechanisms maintaining the abrupt parapatric boundary between the two tick species. Predators may contribute to preventing the more susceptible Ap. hydrosauri from spreading further north, where bluebush litter is more common, and so predation risk is higher. Predators probably have less influence in preventing Amb. limbatum from spreading further south.     

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

In 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.     

Risk of predation for two reptile tick species

Experiments were conducted in the Mount Mary region of South Australia where the distributions of the two reptile-tick speciesAponomma hydrosauri andAmblyomma limbatum narrowly overlap. Engorged larvae and nymphs were placed in boxes with and without access to predators and left for 1 week. At two out of five sites there was greater loss from open access boxes in replicates during warmer periods of the year. Predation by ants appears to be the most likely explanation for the loss of ticks.     

Mating behaviour and parapatry in two species of Australian reptile tick

Summary Few quantitative studies have examined the ecological consequences of similarities and/or differences in mating behaviour of parapatric species. Reproductive interference occurs between several parapatric species of Australian reptile tick, due to similarities in their mating behaviour (Andrews et al. 1982a). Attempts to determine whether reproductive interference serves to maintain parapatry between Amblyomma limbatum and Aponomma hydrosauri have been hindered because of difficulties in providing conditions conducive to conspecific mating in Amb. limbatum. The present study examined whether off-host and/or onhost temperature influenced the subsequent mating behaviour (i.e. the proportion of females that mate and the time when mating occurs) of these two species. Irrespective of the temperature experienced by ticks prior to host attachment, specific on-host temperatures were needed to induce mating in Amb. limbatum (i.e. host cloacal temperatures >32° C prior to the time of peak mating activity). Significantly more Amb. limbatum females were mated and the time taken by females to mate decreased with increasing on-host temperatures. mating in Ap. hydrosauri occurred over a wider range of on-host temperatures and the time when mating occurred did not alter at different on-host temperatures. In addition, significantly more Ap. hydrosauri males moved and each male made more moves on hosts than did Amb. limbatum males. It is suggested that Ap. hydrosauri may in consequence have a competitive mating advantage over Amb. limbatum at a boundary. Similarities in mating behaviour, on the other hand, increase the probability of reproductive interference, hence reduce the reproductive fitness of colonizing females of both species. We propose that similarities and differences in mating behaviour could play a critical role in the maintenance of parapatric boundaries.     

Microhabitat selection by two reptile ticks at their parapatric boundary

The parapatric boundary between the reptile ticks. Aponomma hydrosauri and Amblyomma limbatum, near Mt Mary, South Australia, coincides with a vegetational ecotone. Samples of litter from each side of the tick boundary showed considerable heterogeneity, but there were consistent differences in the composition and quantity of litter. North of the boundary, where Amb. limbatum is found, there is less litter and an absence of Eucalyptus leaves in the litter. Since the litter retards evaporative water loss, and Ap. hydrosauri is less tolerant of dehydration, reduced litter quantity may reduce the fitness of colonizing Ap. hydrosauri. In laboratory and field trials, larvae and nymphs of both tick species chose litter microhabitats in preference to bare soil, with the exception of fed Ap. hydrosauri larvae which, in trials with litter from north of the boundary, rarely moved from the bare soil. This behaviour may also reduce the fitness of colonizing Ap. hydrosauri. The two species adopted different positions in the litter. Ap. hydrosauri were predominantly found on the surface, at the interface between soil and litter as fed larvae, and on or under the surface as nymphs. Amb. limbatum larvae were more often buried under the surface, while nymphs were found mostly in the litter above the soil surface. Hypotheses to explain the maintenance of the parapatric boundary are discussed in the light of these results.     

Reproductive interference between three parapatric species of reptile tick

Summary Reproductive interference between three species of reptile tick, Aponomma hydrosauri, Amblyomma albolimbatum and Amb. limbatum was investigated. Adults of two species attach together on the same lizard hosts in narrow overlap zones at parapatric boundaries between species, providing opportunities for interference. The possibility of reproductive interference was suggested because of similarities in the sexual communication systems.Three forms of interference were found in laboratory experiments. Firstly male movement to search for sexually receptive females was inhibited when females of two species were present on the same host, probably because of signal interference. Secondly, a nonspecific, short range attractant pheromone led males into non-conspecific courtship attempts which reduced the time for conspecific courtships. Thirdly Amb. albolimbatum males physically blocked the genitalia of female Ap. hydrosauri after unsuccessful non-conspecific courtship attempts. Field data showed this behaviour was common in both Amblyomma species after conspecific matings. Reproductive interference would reduce the fitness of each species in sympatry, and may contribute to the maintenance of the narrow parapatric boundaries.     

Reproductive interactions between two Australian reptile tick species

In South Australia the two tick species Amblyomma limbatum and Aponomma hydrosauri share the same common reptile host species, but have allopatric distributions which abut along a narrow parapatric boundary. Reproductive interference is a mechanism that has previously been suggested could contribute to maintaining the boundary. Populations of each species were established in pens within the range of Aponomma hydrosauri. Pens held either each species alone, or the two species together. The performance of females in those pens was monitored over 28 months. There was no indication that the proportion of attached females which mated and engorged was reduced by the presence of heterospecifics. There was no indication that the time taken to mate, engorge and detach was any longer in the presence of heterospecifics. The experiment did not support the hypothesis that reproductive interference contributes to maintaining the parapatric boundary. However, Amblyomma limbatum in the pens had a shorter season of reproductive activity, and achieved much smaller numbers of reproductive females. This may inhibit successful colonization of cooler habitats to the south of its distribution.     

The impact of tick load on the fitness of their lizard hosts

A survey was conducted of natural populations of the sleepy lizard Tiliqua rugosa in South Australia to determine whether infestation by ectoparasitic ticks reduced their fitness. Between 1982 and 1990, 2183 captures of 824 individual lizards were made in an area where they were infested by the tick Aponomma hydrosauri, and 3668 captures of 586 individual lizards were made in an area where they were infested with the tick Amblyomma limbatum. Lizards with high tick loads in one year tended to have high loads the next year. Longevity of lizards in the study was either not correlated with tick load, or positively correlated. Size achieved was greater amongst lizards with greatest tick load, and lizards in mating pairs had higher tick loads than those never found in pairs. The data do not support the hypothesis that tick load diminishes host fitness.     

Can predators maintain parapatry? Ant distribution across a tick parapatric boundary in South Australia

Abstract Ants were sampled by pitfall traps at 85 sites, 0.5 or 1.0km apart, along six transects across a parapatric boundary between the reptile ticks Aponomma hydrosauri and Amblyomma limbatum near Mt Mary in South Australia. There was no tendency for overall ant density, or for the distribution of any single species of ant, to be related to the tick distribution. Thus the survey found no support for the hypothesis that predation by ants was maintaining the boundary. Along transects there were no correlations between ant and tick densities. Thus the survey found no support for the hypothesis that ant predation was a major factor controlling tick densities. These negative results provide further evidence that single, strong ecological processes cannot explain this well-studied parapatric boundary.     

Host-seeking behaviour by Australian ticks (Acari: Ixodidae) with differing host specificities

Ticks generally detach from their hosts into sites where they are later exposed to host species which may or may not be suitable for infestation. The question of how four species of ixodid ticks, with differing specificities, behave towards such potential host species was examined. Observations of the generalists,Aponomma hydrosauri andAmblyomma limbatum and the specialists,Aponomma fimbriatum andAponomma concolor, showed that the generalists were attracted to a wider range of potential host species than the specialists and that the larval stages of all tick species, regardless of specificity, contacted more potential host species than the adults. The interspecific differences may be attributed to reliance on different sets of host cues, while the intraspecific differences may reflect the developmental state of the sensory system.     

Niche segregation in reptile ticks: attachment sites and reproductive success of females

Summary This study examined whether the mating or feeding success of females of two tick species, Amblyomma limbatum and Aponomma hydrosauri, is influenced by their site of attachment on a host. Marked interspecific differences were detected in the preferred sites of attachment of females to their common host, the sleepy lizard Tiliqua rugosa, with Amb. limbatum found predominantly in the ears and on the lower back, while Ap. hydrosauri preferred to attach under the forelimbs and on the midback. Data from field surveys suggested that higher proportions of females were mated in the preferred sites for Ap. hydrosauri, and in one of the preferred sites for Amb. limbatum. However, laboratory and field experiments showed that for both species, the mean time before females were mated, mean engorgement time and mean feeding rate were independent of where they were attached to a host. Four hypotheses were considered as explanations of the observed niche segregation; intespecific competition, avoidance of pheromone jamming or adaptations, to maximize mating and feeding, and minimize physical disturbance. These could not totally explain the observed site specificity in either tick species. Site specificity may represent adaptations by each species to other host species encountered within their distributional range.     

Microhabitat choice and its role in determining the distribution of the reptile tick Amblyomma vikirri

Abstract A newly described tick species, Amblyomma vikirri, infests two lizard species in the Flinders Ranges of South Australia. Although one of the hosts, Tiliqua rugosa, has a wide distribution, the tick distribution is restricted to a subset of rocky habitats where the other host, Egernia stokesii, lives. Experiments were conducted with unfed ticks, the stage when the tick is waiting for a host and is susceptible to desiccation. Amblyomma vikirri had a significantly stronger preference for rock microhabitats than two other tick species (Aponomma hydrosauri and Amblyomma limbatum) that infest T. rugosa. Unfed Amb. vikirri were also more active than the other two species, and more likely to be in the upper pan of the substrate. At warm temperatures, larvae of Amb. vikirri survived for shorter periods under desiccation stress than larvae of the other two species, although as nymphs Amb. vikirri survived as well or better. The rock crevice microhabitat experienced lower maximum temperatures than other potential, non-rock refuge sites. The behaviour of Amb. vikirri, its susceptibility to desiccation in the larval stage and the relatively benign conditions in the rock crevices may act together to prevent Amb. vikirri establishing populations beyond rock habitat.     

The influence of similar aggregation pheromones on the microhabitat choice of two parapatric species of reptile tick (Acari: Ixodidae)

Summary Non-specificity of part of the sex pheromone system of three species of reptile tick has previously been suggested to result in reproductive interference between the species when they attach to the same host (Andrews et al. 1982). Two of the species, Aponomma hydrosauri and Amblyomma limbatum, have common aggregation pheromones which act when the ticks are detached from their hosts. As each species tends to occupy spatially separated microhabitats, the similarity of the aggregation pheromone could lead to interference between species when off their hosts by inducing one species to move away from its preferred microhabitat into that occupied by the other species. This study demonstrates that coaggregations of both species do occur, but that neither species shows a statistically significant shift in microhabitat preference attributable to interactions between species. We suggest that the behaviours leading to microhabitat choice in each species override the influence of the common aggregation pheromone.     

No competition for resources between two tick species at their parapatric boundary

Summary Aponomma hydrosauri and Amblyomma limbatum are tick species with the same major host species, the sleepy lizard Trachydosaurus rugosus, but parapatric distributions in South Australia. Near Mt. Mary one species is abruptly replaced by the other over one kilometre. There is substantial overlap in feeding sites on the hosts. This suggested that interspecific competition, during feeding, may be an important mechanism preventing further overlap of the distributions of the two species. However, in the overlap region there was no resource shortage, and each species infested hosts independently of the other species. Also in laboratory experiments at the highest densities encountered in the field, larvae and nymphs of each species attached and engorged equally well whether alone or mixed with the other species. These data refuted the, hypothesis of interspecific competition between the two species while feeding.     

A non-specific aggregation pheromone in two Australian reptile ticks

Larvae, nymphs, adult males and adult females of each of the Australian reptile tick species Aponomma hydrosauri and Amblyomma limbatum took up significantly aggregated distributions when left for 12 h in the dark in petri dishes. Nymphs of the two species placed together formed co-aggregations. Pheromonal communication was implicated by the attraction of nymphs to filter paper squares which had been in contact with other nymphs. Each species was attracted to pheromone from the other species and no conspecific preference was detected. A common ancestral pheromone is suggested, which may have been retained after speciation by stabilizing selection for a behaviour of major importance to tick survival.     

The impact of tick parasites on the behaviour of the lizard Tiliqua rugosa

Populations of the Australian sleepy lizard, Tiliqua rugosa, near Mt. Mary, South Australia carry natural infestations of two tick species Aponomma hydrosauri and Amblyomma limbatum. In field experiments at two sites, 18 km apart, lizards with experimentally increased tick loads had smaller home ranges, moved shorter distances in a day, and were found basking more but moving less often than lizards from which ticks were experimentally removed. The results were consistent for adult lizards in two years, and for sub-adults in a third year. Laboratory trials showed that juvenile lizards that had tick infestations had lower sprint speeds than uninfested siblings, and that adults with tick infestations had less endurance than those that were uninfested. The results contrast with those of a previous survey that showed that lizards with high tick loads had greater body size and remained longer at a site, but indicate that there may be a balance, for lizards, between the fitness advantages in occupying habitats with high-quality resources, and the costs from parasites that also prefer those habitats. Received: 02 March 1999 / Accepted: 07 October 1999     

Ticks (Acari: Ixodidae) within various phytophysiognomies of a Cerrado reserve in Uberlandia, Minas Gerais, Brazil

Cerrado biome, the South American savannah, covers about 2 million km² and is very rich in endemic species but threatened by agriculture. In this report free-living tick species are presented, and their seasonal and relative distribution within the various phytophysiognomies in a small Cerrado reserve in Minas Gerais State, Brazil. Overall 2,694 free-living ticks were found during a 2 years sampling period with CO₂ traps and cloth dragging. Of these, 73.5% were Amblyomma cajennense and 0.6% Amblyomma dubitatum. All other ticks (25.9%) were retained as Amblyomma spp. Adults of A. cajennense peaked in spring, the nymphs in winter of both years. Amblyomma larval clusters were found in autumn and winter. Adult ticks (46.7%) and nymphs (39.5%) were most often found in woodlands, whereas most larval clusters were found in valley-side marshes (39%). Amblyomma cajennense, Anocentor nitens, Rhipicephalus (Boophilus) microplusand Rhipicephalus sanguineus ticks were found on domestic animals from neighboring properties. Search for Rickettsia in the hemolymph of 497 A. cajennense and one A. dubitatum ticks yielded negative results. Results confirmed earlier reports on the overwhelming prevalence of A. cajennense ticks in the Cerrado biome of Brazil and added information to habitat preferences of this tick species, a major vector in Brazil of the Rocky Mountain spotted fever.