Tiliqua Rugosa Research Articles

The use of body condition and haematology to detect widespread threatening processes in sleepy lizards (Tiliqua rugosa) in two agricultural environments

Agricultural practices, including habitat alteration and application of agricultural chemicals, can impact wildlife resulting in their decline. Determining which of these practices are contributing to declines is essential if the declines are to be reversed. In this study, the health of two geographically separated sleepy lizard (Tiliqua rugosa) populations was compared between a rangeland environment and cropping environment using linear body size index (LBSI) and haematology. Animals in the cropping site were smaller, suggesting genetic differences as the result of geographical isolation. The animals in the cropping site had a lower LBSI and many were experiencing a regenerative anaemia. The anaemia was postulated to be the cause of the low LBSI. The anaemia appeared to be the result of haemolysis and was likely to be caused by exposure to agricultural chemicals applied in the cropping site but not the rangeland site. Elevated white blood cell counts in lizards in the rangeland site suggested that they were experiencing an inflammatory disease of possible ecological significance. Together, these results demonstrate the value of combining physical and haematological parameters when studying the impact of agricultural practices on wildlife. They also show that reptiles may be useful as sentinel species for livestock and humans.

A contact-based social network of lizards is defined by low genetic relatedness among strongly connected individuals

Social organization is widespread; even largely solitary species must organize themselves to enable contacts with mates and reduce competition with conspecifics. Although the forms of social structure can be subtle in solitary species, understanding the factors that influence them may be important for understanding how different forms of social organization evolved. We investigated the influence of genetic relatedness and spatial structure on social associations in a solitary living Australian scincid lizard, Tiliqua rugosa. We derived the genetic relatedness of 46 lizards from analysis of genotypes at 15 microsatellite DNA loci, and described social networks from GPS locations of all the lizards every 10. min for 81 days during their main activity period of the year. We found that connected male dyads were significantly more related than expected by chance, whereas connected male-female and female-female dyads had lower relatedness than expected. Among neighbouring male-male and male-female dyads, the strongest social relationships were between lizards that were the least related. Explanations of this pattern may include the avoidance of inbreeding in male-female dyads, or the direction of aggressive behaviour towards less related individuals in male-male dyads. Observed social associations (inferred through synchronous spatial proximity) were generally lower than expected from null models derived from home range overlap, and many close neighbours did not make social contact. This supports our hypothesis for the presence of deliberate avoidance between some neighbouring individuals. We suggest that lizards can discriminate between different levels of relatedness in their neighbours, directing their social interactions towards those that are less related. This highlights differences in how social associations are formed between species that are solitary (where associations form between unrelated conspecifics) and species that maintain stable social groups structured by kinship.

Reptile bycatch in a pest-exclusion fence established for wildlife reintroductions

Conservation fences have been used as a tool to stop threatening processes from acting against endangered wildlife, yet little is known of the impacts of fences on non-target native species. In this study, we intensively monitored a pest-exclusion fence for 16 months to assess impacts on a reptile community in south-eastern Australia. We registered 1052 reptile records of six species along the fence. Encounters and mortality were greatest for eastern long-necked turtles (Chelodina longicollis), whereas impacts on lizards (Tiliqua rugosa, Tiliqua scincoides, Pogona barbata, Egernia cunninghami) and snakes (Pseudonaja textilis) were more moderate. We recorded several Chelodina longicollis recaptures at the fence and many of these were later found dead at the fence, indicating persistent attempts to navigate past the fence. We conservatively estimate that the fence resulted in the death of 3.3% and disrupted movements of 20.9% of the turtle population within the enclosure. Movement disruption and high mortality were also observed for turtles attempting to enter the nature reserve, effectively isolating the reserve population from others in the wider landscape. Of 98 turtle mortalities, the most common cause of death was overheating, followed by predation, vehicular collision, and entanglement. Turtle interactions were clustered in areas with more wetlands and less urban development, and temporally correlated with high rainfall and solar radiation, and low temperature. Thus, managers could focus at times and locations to mitigate impacts on turtles. We believe the impact of fences on non-target species is a widespread and unrecognized threat, and suggest that future and on-going conservation fencing projects consider risks to non-target native species, and where possible, apply mitigation strategies that maintain natural movement corridors and minimize mortality risk.

Random non-coding fragments of lizard DNA: anonymous nuclear loci for the Australian skink, Tiliqua rugosa, and their utility in other Egernia-group species

We report the development of 48 anonymous nuclear loci from the Australian skink Tiliqua rugosa using 454 sequencing. These loci amplified across a Western Australian lineage (47 loci), a ‘northern’ lineage (48 loci) and a ‘southern’ lineage (46 loci). We further tested amplification for the related T. adelaidensis and Egernia stokesii where 37 and 34 loci amplified respectively. The loci showed variability within T. rugosa (22 polymorphic loci) and at least 27 loci also exhibited variation among the three species, highlighting the usefulness of these markers for phylogenetic, phylogeographic and population genetic analyses in T. rugosa and related species.

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.

The response of a sleepy lizard social network to altered ecological conditions

The use of social networks to describe animal social structure is increasing, yet our understanding of how social networks respond to changing ecological conditions remains limited. Animal behaviour is often constrained by temporal or spatial variation in ecological conditions; how do behaviour and social organization respond to changing ecological conditions? We used a social network approach to ask this question in the pair-living sleepy lizard, Tiliqua rugosa. We attached GPS data loggers to lizards to record their movement, activity and social interactions during their activity period (October–December) in 2008–2010. The years varied substantially in ecological conditions, from hot and dry in 2008 to cool and wet in 2010. Our aim was not to suggest how individual climatic or ecological factors influence social organization, but to explore the stability of social structure over varying conditions. Lizards spent less time active and overlapped in home range area more with conspecifics in the driest year of the study (2008) than in subsequent years. Despite this variation in behaviour, the number and strength of connections in the social network were stable across years. Intrasexual associations were similar across years, but there was a lower incidence of intersexual associations in 2008 than in the other 2 years. Among male–female dyads, pairing intensity was lower in 2008, while for males, extrapair strength was higher in 2008. These results suggest that although the overall social network is tolerant to changes in ecological conditions, the nature of contacts within the network shifts in response to ecological variation.

Arthropod Intermediate Hosts ofAbbreviata antarctica(Nematoda: Physalopteridae) in Australia

This study examines potential arthropod intermediate hosts for the nematode Abbreviata antarctica. Five species of arthropod (tropical native cricket Teleogryllus oceanicus; native roach Drymoplaneta communis; native termite Nasutitermes exitiosus; and 2 introduced species, the East African roach Naupheta cinerea and the Asian cricket Acheta domesticus) were fed feces from a skink, Tiliqua rugosa, containing embryonated eggs of A. antarctica . The insects were dissected at 4 intervals (1 day, 4 days, 8-16 days, and 25-26 days). Viable third-stage larvae were recovered from cysts on the external wall of the midgut and hindgut of 62.5% nymphal and adult T. oceanicus crickets at 25-26 days post-infection and from a single nymphal A. domesticus cricket. No roaches contained eggs or first-stage larvae after 48 hr, and neither eggs nor larvae were found in termites.

Eimeria tiliquae n. sp. (Apicomplexa: Eimeriidae) from the shingleback skink (Tiliqua rugosa rugosa)

A new species, Eimeria tiliquae n. sp. is described from a shingleback skink (Tiliqua rugosa rugosa). Sporulated oocysts (n=50) are spherical to subspherical, with colourless trilaminate oocyst wall, 0.7±0.1 (0.5-0.75) thick. Oocyst with 4 spheroidal to subspheroidal sporocysts. Oocyst length, 13.7±0.9 (12.0-16.3); oocyst width, 12.8±0.9 (11.5-15.0); oocyst length/width (L/W) ratio, 1.07±0.05 (1.0-1.2). Micropyle, oocyst residuum and polar granule absent. Sporocysts with globular sporocyst residuum and 2 sporozoites. Sporocyst length, 6.0±0.6 (5.0-7.5); sporocyst width, 5.4±0.6 (4.0-7.0); sporocyst L/W ratio, 1.11±0.11 (1.0-1.5). Stieda, parastieda and substieda bodies absent. Phylogenetic analysis of 18S rRNA sequences indicated that E. tiliquae n. sp. shared 96.4-96.5% genetic similarity to E. tropidura, its closest relative. Reptile-derived sequences were not available for the mitochondrial cytochrome oxidase gene (COI) and phylogenetic analysis at this locus placed E. tiliquae n. sp. in a clade by itself but grouping closest (92% similarity) with a novel isolate from a King's skink (Egernia kingii) from Western Australia. Based on morphological and molecular data, this isolate is a new species of coccidian parasite that to date has only been found in shingleback skinks.

Ocular Anatomy and Retinal Photoreceptors in a Skink, the Sleepy Lizard (Tiliqua rugosa)

The Australian sleepy lizard (Tiliqua rugosa) is a large day-active skink which occupies stable overlapping home ranges and maintains long-term monogamous relationships. Its behavioral ecology has been extensively studied, making the sleepy lizard an ideal model for investigation of the lizard visual system and its specializations, for which relatively little is known. We examine the morphology, density, and distribution of retinal photoreceptors and describe the anatomy of the sleepy lizard eye. The sleepy lizard retina is composed solely of photoreceptors containing oil droplets, a characteristic of cones. Two groups could be distinguished; single cones and double cones, consistent with morphological descriptions of photoreceptors in other diurnal lizards. Although all photoreceptors were cone-like in morphology, a subset of photoreceptors displayed immunoreactivity to rhodopsin-the visual pigment of rods. This finding suggests that while the morphological properties of rod photoreceptors have been lost, photopigment protein composition has been conserved during evolutionary history.

Social networks and the spread of Salmonella in a sleepy lizard population

Although theoretical models consider social networks as pathways for disease transmission, strong empirical support, particularly for indirectly transmitted parasites, is lacking for many wildlife populations. We found multiple genetic strains of the enteric bacterium Salmonella enterica within a population of Australian sleepy lizards (Tiliqua rugosa), and we found that pairs of lizards that shared bacterial genotypes were more strongly connected in the social network than were pairs of lizards that did not. In contrast, there was no significant association between spatial proximity of lizard pairs and shared bacterial genotypes. These results provide strong correlative evidence that these bacteria are transmitted from host to host around the social network, rather than that adjacent lizards are picking up the same bacterial genotype from some common source.

Causes and consequences of sleepy lizard, Tiliqua rugosa, social networks

Causes and consequences of sleepy lizard, Tiliqua rugosa, social networks

Gestation increases the energetic cost of breathing in the lizard, Tiliqua rugosa

High gestational loads result in fetuses that occupy a large proportion of the body cavity and may compress maternal organs. Compression of the lungs results in alterations in breathing patterns during gestation, which may affect the energetic cost of breathing. In this study, the energetic cost of breathing during gestation was determined in the viviparous skink Tiliqua rugosa. Radiographic imaging showed progressive lung compression during gestation and a 30% reduction in the lung inflation index (rib number at which the caudal margin of the lung was imaged divided by total rib number). Pneumotachography and open flow respirometry were used to measure breathing patterns and metabolic rates. Gestation induced a twofold increase in minute ventilation via increases in breathing frequency, but no change in inspired tidal volume. The rates of O(2) consumption and CO(2) production did not change significantly during gestation. Together, these results suggest that a relative hyperventilation occurs during gestation in T. rugosa, which in turn suggests that diffusion and/or perfusion limitations may exist at the lung during gestation. The energetic cost of breathing was estimated as a percentage of resting metabolic rate using hypercapnia to stimulate ventilation at different stages of pregnancy. The energetic cost of breathing in non-pregnant lizards was 19.96±3.85% of resting metabolic rate and increased threefold to 62.80±10.11% during late gestation. This significant increase in the energetic cost of breathing may have significant consequences for energy budgets during gestation.

A direct benefit of native saltbush revegetation for an endemic lizard (Tiliqua rugosa) in southern Australia

Land alteration for intensive agriculture has been a major cause of species decline and extinction globally. In marginal grazing regions of southern Australia, native perennial shrubs are increasingly being planted to supplement pasture feeding of stock. Such revegetation has the benefits of reducing erosion and salinity, and importantly, the potential provision of habitat for native fauna. We explored the use of revegetated native saltbush by the sleepy lizard (Tiliqua rugosa) an endemic Australian species common in the region. We repeatedly sampled revegetated saltbush throughout 2010 and 2011 for adults (n = 55) and juveniles (n = 26). Using genotypes from eight microsatellite loci, parents were assigned to half of all juveniles with high statistical confidence. Parents were sampled in the same patch of revegetated saltbush as their offspring, thus supporting the observation that juvenile sleepy lizards remain within the home range of their parents before dispersal. Most importantly, our findings indicate that revegetated saltbush provides important habitat for T. rugosa at significant life stages – before and during breeding for adults, and before dispersal for juveniles. We conclude that revegetation using simple, monoculture plantations provides beneficial habitat for T. rugosa and may also be beneficial habitat for other native species in human-altered agricultural landscapes.

Lovers and fighters in sleepy lizard land: where do aggressive males fit in a social network?

In this study we explored relationships between the aggressiveness of male sleepy lizards, Tiliqua rugosa, and their position in a social network. We attached activity loggers to 60 neighbouring lizards during the activity season (September–December) in 2009 at a study site in the mid-north of South Australia. The loggers continuously recorded the activity and location of lizards, allowing us to infer direct social associations. We calculated pairwise associations and integrated these into a social network and calculated node-based measures that quantified male–male and male–female interactions. Aggressiveness of males was quantified in two ways; by involvement in a fight, as indicated by the presence of fresh scale damage, and by aggression assays that scored the response of lizards to conspecific and predator cues. More aggressive lizards in these assays were more likely to be found with fresh scale damage in field surveys. Less aggressive males were more strongly connected to females in the network, and were more commonly in contact with their monogamous female partner, than more aggressive males. Our results suggest a behavioural syndrome among male lizards connecting level of aggression and association with females, with a divergence in behaviour; lovers that are strongly paired and nonaggressive, and fighters that are weakly associated with females and more aggressive.

Pair-living in the Absence of Obligate Biparental Care in a Lizard: Trading-off Sex and Food?

A pair-living social organisation can typically be explained by obligate biparental care. We investigated pair-living in the absence of biparental care in the Australian sleepy lizard, Tiliqua rugosa, which forms exceptionally strong pair bonds. We fitted 10 lizards, five male–female pairs, with Global Positioning System (GPS) recorders and continuously monitored social associations and separations between active pair partners, based on location records taken every 10 min over 3 mo. Males temporarily separated and reunited the pair more frequently than females, but females also contributed to the maintenance of the pair bond. These behavioural data were consistent with the hypothesis that females successfully coerce males into associations with one female. Lower frequencies of social association between pair partners once mating had finished support this interpretation. Males that are coerced into pair associations appear to experience higher costs of pair-living than females, because males initiated temporary separations of the pair more frequently than females. Males showed higher movement activity and remained active later each day. This sex bias in activity may be an important mechanism to mitigate the higher costs of pair-living for males. Costs for males might include within-pair competition for food as females appear more competitive. Our study provides detailed empirical data on a lizard pair bond and provides important insights into pair-living in the absence of biparental care.

Retinal ganglion cell topography and visual acuity of the sleepy lizard (Tiliqua rugosa)

The spatial distribution of retinal ganglion cells provides valuable insight into the importance species place on observing objects in specific regions of their visual field with higher spatial resolving power. We estimate the total number, distribution and peak density of ganglion cells in retinal wholemounts of the sleepy lizard, Tiliqua rugosa, a scincid lizard endemic to southern Australia. Ganglion cells were readily discernable from amacrine cells by their size and shape, prominent nuclei and the accumulation of Nissl-positive substances in their cytoplasm. A total of 1,654,200 (±59,400) presumed ganglion cells were estimated throughout the retina, distributed irregularly and forming a loose horizontal streak of high cell density peaking at 15,500 cells per mm(2). With a post nodal distance of 6.25 mm, we calculate an upper limit of visual acuity of 6.8 c/deg.

Late Pleistocene Egernia group skinks (Squamata: Scincidae) from Devils Lair, Western Australia

Research on squamate evolution of Australia has predominantly focused on the eastern portion of the continent, whereas little is known about the record from Western Australia. Deposits in Devils Lair provide a glimpse of late Pleistocene Egernia group skink representation from the Cape Leeuwin-Naturaliste region of southwestern Western Australia. Previous studies of fossils from the cave indicate a peak in the number of lizard remains during the last glacial maximum, a time when mammal and charcoal remains suggest an open, dry environment. Previous studies of Devils Lair have not attempted to identify lizard remains beyond ‘lizard’. Here, we identify Egernia group lizard remains as Liopholis spp., Egernia spp., Lissolepis spp. and Tiliqua rugosa, which range in age from ca 48 000 to 13 000 yr B.P.

Forestcheck: terrestrial vertebrate associations with fox control and silviculture in jarrah (Eucalyptus marginata) forest

Summary Terrestrial vertebrate associations with silviculture and other factors were investigated as part of the FORESTCHECK monitoring program in the jarrah (Eucalytpus marginata) forests of south-west Western Australia. A total of 48 integrated monitoring grids form the basis of this study—sampled over five years (2001–2006), across five ecosystem-defined regions (one sampled per year), each with replicates of two silvicultural treatments (shelterwood, gap release) and external reference forest (uncut forest or structurally mature forest that had not been harvested for timber for over 40 y). Terrestrial vertebrates were surveyed in spring and autumn using pitfall traps and wire cages. Forty-one terrestrial vertebrate taxa (8 frogs, 22 reptiles, 11 mammals) comprising 1165 captures were recorded. Fox (Vulpes vulpes) control had the strongest effect on terrestrial vertebrates, with baited areas supporting significantly more individuals (three-fold increase) than unbaited areas. The mammals Trichosurus vulpecula, Bettongia penicillata, Cercartetus concinnus and Dasyurus geoffroii, and the skink Tiliqua rugosa were particularly more abundant in fox-baited forest. Several terrestrial vertebrate community attributes (species accumulations by grids and number of individuals, dominance-diversity plots, overall community structure and overall abundance) differed little among the three treatments (i.e. two silvicultural, plus external reference forest). However, external reference grids had significantly lower species richness than the shelterwood grids and a significantly different community structure. These differences resulted from a greater prevalence within shelterwood of some species such as the reptiles Egernia napoleonis, Menetia greyii, Ctenotus labillardieri and Ramphotyphlops australis. Forests that had never been harvested, a subset (8/15 grids) of the external reference treatment, had the lowest overall abundance, due largely to a confounding with fox control. The level of replication enabled differences between treatments of greater than 23% in species richness, and 37% in overall abundance, to be detected as statistically significant. Significant ecosystem/year differences were found. Differences in community structure between ecosystems/years approximated the geographic/bioclimatic relationships between the grids, with the distinction between southern jarrah communities (Jarrah South/2001–02 and Jarrah Blackwood Plateau/2005–06) and the northern communities being particularly apparent. Time since last fire, live tree basal area, and the proportion of basal area removed by harvesting and silvicultural treatment were not correlated with vertebrate species richness, abundance or community structure. In comparison to the effect of fox control and regional/temporal variation, silvicultural treatment and the intensity of timber harvesting had minor impacts. Suggestions for the improvement of this and similar studies are discussed, with a particular focus on reducing residual variance and increasing sample size.

The influence of refuge sharing on social behaviour in the lizard Tiliqua rugosa

Refuge sharing by otherwise solitary individuals during periods of inactivity is an integral part of social behaviour and has been suggested to be the precursor to more complex social behaviour. We compared social association patterns of active versus inactive sheltering individuals in the social Australian sleepy lizard, Tiliqua rugosa, to empirically test the hypothesis that refuge sharing facilitates social associations while individuals are active. We fitted 18 neighbouring lizards with Global Positioning System (GPS) recorders to continuously monitor social associations among all individuals, based on location records taken every 10 min for 3 months. Based on these spatial data, we constructed three weighted, undirected social networks. Two networks were based on empirical association data (one for active and one for inactive lizards in their refuges), and a third null model network was based on hypothetical random refuge sharing. We found patterns opposite to the predictions of our hypothesis. Most importantly, association strength was higher in active than in inactive sheltering lizards. That is, individual lizards were more likely to associate with other lizards while active than while inactive and in shelters. Thus, refuge sharing did not lead to increased frequencies of social associations while lizards were active, and we did not find any evidence that refuge sharing was a precursor to sleepy lizard social behaviour. Our study of an unusually social reptile provides both quantitative data on the relationship between refuge sharing and social associations during periods of activity and further insights into the evolution of social behaviour in vertebrates.

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.