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.     

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.     

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.     

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.     

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.     

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.     

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.     

Effect of delayed mating and prolonged engorgement on the reproductive fitness of female Amblyomma limbatum (Acari: Ixodidae) in marginal population areas

Reptile ticks mate while females are attached to their host. Following mating, females engorge, detach and then lay their eggs. This study examines whether the time that females of the reptile tick Amblyomma limbatum spend on hosts prior to mating and the time they take to engorge on hosts after mating influence their reproductive fitness, as measured by the number of viable eggs they produce. When compared with females that experienced no temperature-induced delay in mating, females attached for an initial period to hosts with body temperatures too low to induce mating had no decline in their reproductive fitness, once provided with suitable temperatures for mating. However, on hosts with suitable body temperatures for mating, female ticks that took longer to mate, took longer to engorge and had reduced reproductive fitness. In addition, females that spent more than 20 days feeding on hosts after mating had reduced reproductive fitness, irrespective of the time they spent on hosts prior to mating compared with females with shorter feeding periods. Thus, the time that A. limbatum females spent on hosts prior to mating and/or after mating has a significant bearing on the number viable progeny produced. The ecological implications of these results are discussed in relation to females colonizing marginal population areas at the edge of their distributional range.     

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.     

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.     

Interspecific differences in the movements of female ticks on reptiles.

Movements of females of two reptile ticks, Amblyomma limbatum and Aponomma hydrosauri were studied to determine whether the behaviour of the species on hosts was similar or different. Experiments were conducted to determine if the movement of females on hosts prior to mating was influenced by the delayed attachment of conspecific males. A field experiment was also undertaken to determine whether data obtained during laboratory experiments reflected the behaviour of females on hosts in the field. Both in laboratory and field experiments, a significantly greater proportion of Ap. hydrosauri females changed their site of attachment prior to mating. Individual Ap. hydrosauri females made significantly more positional changes than Amb. limbatum females. These interspecific differences occurred irrespective of the absence of conspecific males or presence of non-conspecific adults on hosts. These data may have important ecological implications in relation to the success of colonizing females at their parapatric boundary.     

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.     

Mating behaviour and reproductive isolation of three species of reptile tick

The mating behaviour of three species of reptile tick, Aponomma hydrosauri, Amblyomma albolimbatum and Amb. limbatum is similar and involves a female sex pheromone which activates males to detach from their hosts and search. After contacting females, a stereotyped six-phase courtship sequence occurs. There are qualitative differences between the species in courtship behaviour at phase 3 (reversal of position by dorsally mounted males) and phase 6 (the copulation position). On-host observations of non-conspecific mating show that females of the three species have species-specific activation pheromones, which is contrary to reports in other species of tick. Such specificity should result in reproductive isolation of the three species; however, under certain circumstances it may not prevent non-conspecific contacts between the sexes. Off-host observations of courtship behaviour show that once males of the three species contact non-conspecific females, they attempt courtship and are persistent with their courtship. Rarely did non-conspecific courtships proceed beyond phase 4 of the courtship sequence, as non-conspecific females did not lift their bodies to allow males venter contact. Differences between the species in leg orientation in the copulation position, together with body size differences, are responsible for a complete barrier to successful non-conspecific copulation. The observations illustrate the role that behavioural mechanisms play in reproductively isolating these three species of tick.     

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.     

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

Perhaps 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.     

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.     

Reproductive interference, priority effects and the maintenance of parapatry in Skistodiaptomus copepods

Reproductive interactions among species, such as attempts to mate with heterospecifics, can have profound impacts on patterns of geographic range and co-occurrence. For example, several theoretical models demonstrate that reproductive interference-the negative influence of heterospecifics on the abilities of conspecifics to successfully mate-can lead to parapatry, even across homogeneous landscapes, when the parapatric species are initially allopatric. However, the potential consequences of reproductive interactions on patterns of range limits and co-occurrence have been largely ignored by ecologists. Here, I use a combination of laboratory mating experiments and a genetic survey for two parapatric species of Skistodiaptomus copepods to evaluate the potential importance of interspecific reproductive interactions on the maintenance of parapatry. The genetic survey demonstrates phylogenetic exclusivity of these species, suggesting that gene flow has not occurred between them. Moreover, laboratory crosses between both species demonstrate that their parapatric boundary is not maintained as a hybrid zone because the two species cannot form viable hybrids. However, Skistodiaptomus oregonensis and S. pygmaeus males mate indiscriminately and interfere with the ability of heterospecific females to successfully reproduce. I suggest that reproductive interference results in priority effects that strongly influence the maintenance of this parapatric boundary and stress that reproductive traits are important and often-overlooked in ecological models for species range limits.     

Short‐Term Nutritional Limitation Affects Mating Behaviour and Reproductive Output in Dwarf Spiders

Mating decisions can vary considerably depending on individual experience, mate availability and nutritional status. Here, we applied short‐term dietary restrictions to adult female spiders that were well fed during the juvenile stage in an effort to understand whether and how brief periods of food shortage can influence male and female mating decisions and mating behaviour. To assess whether responses vary between closely related species, we conducted the same experiment on the dwarf spiders Oedothorax retusus and O. apicatus. During courtship and mating, males of both species offer secretion to females from glandular tissue in their prosoma. Females were subject to food shortage over a period of 3 wks (‘low‐diet’ treatment, LD) or fed regularly (‘high‐diet’ treatment, HD). We compared courtship probability, mating probability/behaviour, and reproductive output between dietary groups and species. In both Oedothorax species, females in the LD treatment were less likely to mate and more aggressive towards males. Furthermore, LD females produced egg sacs that were significantly lighter than were those of the HD females. Effects of food deprivation on copulation duration, gustatory behaviour and oviposition latency differed between species. Our study shows that short periods of dietary restriction during the adult stage can strongly affect mating behaviour and reproductive output with differences between closely related species.     

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.     

Sex in a cyclical parthenogen: mating behaviour of Chydorus sphaericus (Crustacea; Branchiopoda; Anomopoda)

1. We describe the interactions during mating in Chydorus sphaericus, a cyclical parthenogenetic anomopod. Mating behaviour is more complex than previously assumed, with evidence for a diffusible chemical to which males react at the onset of mating, for reproductive isolation, and for postcopulatory mate guarding. 2. During mating, the male and female form a ‘mating cross’ that may be maintained for several hours, while copulation itself typically lasts less than a minute. Furthermore, males invariably attach to the right valve of females. Copulation involves intromission of the postabdomen between the valves, so that the gonopores approach the left ovarium. 3. This behaviour is reflected in the morphology of both sexes: males have a specialised anterior valve margin, postabdomen, first limb and rostrum, under selective pressure for successful mate guarding and copulation, while gamogenetic females have asymmetric ovaries, and a species‐specific setulation of the valves. Males of the structurally related Chydorus ovalis react to the presence of C. sphaericus, but fail to dock to females, suggesting a lock‐antilock element in the reproductive isolation of both species. 4. The morphological and ethological adaptations in C. sphaericus suggest that there is a strong selective pressure on mating behaviour in this cyclical parthenogen and specifically towards the formation of the ‘mating cross’.