Pygmy Bluetongue Lizard Research Articles

Editorial for the Michael Bull special issue

A review of the role of parasites in the ecology of reptiles and amphibiansParasite in peril? A new species of mite in the genus Ophiomegistus Banks (Parasitiformes: Paramegistidae) on an endangered host, the pygmy bluetongue lizard Tiliqua adelaidensis (Peters) (Squamata: Scincidae)

Translocation for conservation: Neonates are less suitable than adults

AbstractAnimal behaviour can affect the outcome of conservation translocations. It is important to understand the behaviour of the species being considered for translocation and how its behaviour varies over life stages. There may be uncertainty about what life stages are best as founders for release back into wild populations. A technique called head‐starting whereby juvenile life stages are raised in captivity and then released is one potential pre‐release strategy. However, juveniles of many species have a dispersive role in the life cycle, potentially raising difficulties for establishing new populations due to dispersal from the intended habitat following release. For this study, we compared aspects of the behaviour of captive adult and neonate pygmy bluetongue lizards (Tiliqua adelaidensis) – an endangered species for which translocation is likely to be an important management strategy – to determine if neonate behavioural characteristics are appropriate for their translocation. We filmed adult and neonate pygmy bluetongue lizards and compared their behaviour. We also filmed adults over an activity season to compare seasonal behaviour. Behavioural parameters measured included basking time, burrow exits, burrows occupied and walking the perimeter wall. Neonates basked significantly more than adults in summer and autumn. Neonates are likely to be basking more than adults because they are in a stage of rapid growth and need to gain body mass before the winter inactivity period. Neonates exited burrows more often than adults and used a greater number of burrows. These results indicate neonate lizards are actively exploring their habitat. Neonates are unlikely to be as suitable for translocation as they are actively moving about and more likely to be predated upon or disperse from the translocation site. Our finding can be applied to other species that have active juvenile life stages and are at particular risk of predation due to their small size.

Recognition of reptile predator scent is innate in an endangered lizard species

Chemical cues can alert prey to the presence of predators before the predator is within visual proximity. Recognition of a predator’s scent is therefore an important component of predator awareness. We presented predator and control scents to wild, wild-born captive, and predator-naive captive-born pygmy bluetongue lizards to determine (1) whether lizards respond to reptile chemical cues differently from controls, (2) whether captive lizards respond more strongly to a known predator than to other predatory reptiles, (3) whether captive-born lizards recognise predators innately, whether captive-born lizards have reduced predator recognition compared with wild lizards and whether time spent in captivity reduces responses to predators, and (4) whether the avoidance response to predator detection differs between naive and experienced lizards. There was no significant difference in the number of tongue flicks to predator scent among wild, wild-born and captive-born lizards, suggesting that predator detection is innate in the pygmy bluetongue lizard and time in captivity did not reduce predator recognition. The number of tongue flicks directed towards brown snake scent was significantly higher than that to the novel and water controls for all lizard origins. Lizards of all origins continued to bask in the presence of predator scents, suggesting that chemical cues alone may be insufficient to instigate an avoidance response and other cues may be required.

Effects of grazing regime on the relative body mass of the endangered pygmy bluetongue lizard (Tiliqua adelaidensis)

AbstractMany animals rely on fat reserves, to keep them alive through extended periods of food shortage, such as the winter, and to provide additional energy for reproduction. Fat reserves, measured relative to an animal's size, are often referred to as the animal's body condition. The present study investigated how different levels of grazing by domestic stock in native grassland habitat affect the body condition of the pygmy bluetongue lizard (Tiliqua adelaidensis), and if these effects are related to changes in the abundance and size of grasshoppers which are the lizards primary source of food. The initial hypothesis was that lizards would have the highest body condition in moderately grazed paddocks, because those paddocks would have more grasshoppers than heavily grazed paddocks, and better visual conditions for lizards to catch those grasshoppers than in ungrazed paddocks. The results, however, showed that both lizard body condition and the abundance of grasshoppers increased with decreasing grazing intensity. The connection between lizard body condition and abundance of grasshoppers was complex. Within an activity season, lizard body condition generally declined from spring to summer, while the number of grasshoppers grew. The mean size of grasshoppers seemed to be more important, as lizard body condition was higher in spring, the time of year with the largest grasshoppers. These results show that the intensity of grazing by domestic stock influences the body condition of pygmy bluetongue lizards, but that this effect is not entirely due to the reduction in the number of grasshoppers resulting from grazing.

Population augmentation had no effect on the abundance or body condition of conspecifics and co‐occurring lizard species in a native grassland community

AbstractWildlife translocations have been historically plagued by failure. As more species gain endangered status, we must increase the success rate through use of pre‐emptive empirical, evidence‐based research. The main ecological risk is the potential for the relocated individuals to have competitive advantage at the recipient site, acting invasively and, potentially, outcompeting the native fauna for food, shelter or other resources. Here we investigated the ecological risk of increased population density, following a population augmentation of the pygmy bluetongue lizard (Tiliqua adelaidensis) an endangered lizard, endemic to South Australia. We experimentally increased T. adelaidensis density to ascertain if a sudden increase in T. adelaidensis density would negatively affect the abundance or body condition of the resident conspecifics and co‐existing lizard species found at the recipient site. Twenty‐four individuals, from two populations, were relocated into previously built enclosures at a recipient site in grassland habitat, north of Adelaide, South Australia. For one activity‐season pre and post the augmentation, co‐existing lizard species were sampled in an effort to detect any changes inabundance or body condition. Comparisons were also made between experimental enclosures, containing residents and translocated individuals and control enclosures, containing only residents. Using Menetia greyii as a proxy for all of the competing species, our results show there was no reduction in abundance or body condition post augmentation. Our lack of evidence indicating a negative impact of the T. adelaidensis translocation on the body condition and abundance of the resident lizard species is a positive outcome for future conservation of this species. This study provides a new way of approaching wildlife movements, through identification of potential risks using small‐scale translocations in an enclosed area before conducting large‐scale releases into unfenced areas; the results are intended to facilitate higher translocation success rates and limit the negative effects upon the wider ecological community at recipient sites.

Co‐occupancy of spider‐engineered burrows within a grassland community changes temporally

AbstractBurrow‐digging organisms act as ecosystem engineers, providing potential habitat to other organisms. In the Mid North region of South Australia, wolf and trapdoor spiders in fragmented grassland communities provide this service. Pygmy bluetongue lizards are an endangered skink, endemic to these grasslands. The lizards obligatorily use burrows dug by these spider groups as refuges, basking sites and ambush points. We investigated the occupancy of these spider burrows by lizards and other organisms within the grassland community, identifying the occasions that burrows were shared by multiple taxa. We found that the lizards and trapdoor spiders are predominantly solitary, while wolf spiders co‐shared burrows more frequently with either weevils or snails. There were numerous taxa that were found to regularly co‐share with other taxa, particularly snails, centipedes and weevils. There was a strong temporal influence on burrow sharing, with most co‐sharing occurring late in summer. This study provides an insight into the use of burrows by the lizards and co‐existing taxa within these grassland communities. The dynamics of burrow‐use by other taxa have the potential to influence long‐term conservation of these lizards as burrow availability is crucial to their survival in these grasslands.

Parasite in peril? A new species of mite in the genus Ophiomegistus Banks (Parasitiformes: Paramegistidae) on an endangered host, the pygmy bluetongue lizard Tiliqua adelaidensis (Peters) (Squamata: Scincidae)

AbstractHost‐parasite relationships are generally understudied in wild populations but have a potential to influence host population dynamics and the broader ecosystem, which becomes particularly important when the host is endangered. Herein we describe a new species of parasitic mite from the genus Ophiomegistus (Parasitiformes: Mesostigmata: Paramegistidae) of an endangered South Australian skink; the pygmy bluetongue lizard (Tiliqua adelaidensis). Adult mites were observed on lizard hosts in three different host populations, among which prevalence varied. No temporal trend in prevalence was evident over two spring‐summer seasons of monitoring. We hypothesise that the reliance on burrows as refuges by T. adelaidensis may be essential for the completion of the mite life cycle and also for horizontal transmission. The conservation implications of not only its effect on the host, but also its potential status as an endangered species itself, are considered.

Does sheep grazing affect burrow choice of the pygmy bluetongue lizard (Tiliqua adelaidensis)?

The pygmy bluetongue lizard (Tiliqua adelaidensis) inhabits burrows originally dug by spiders in a few remaining fragments of native Australian grassland. These fragments are typically invaded by exotic plant species and subject to livestock grazing. We predicted that lizards prefer burrows in areas with reduced vegetation cover that will allow them to bask and see their invertebrate prey. We applied alternative grazing regimes to six experimental paddocks and found that sheep reduced vegetation density proportionally to the grazing intensity. Within each paddock, independent of the level of grazing, and in seven of the eight surveys, lizard burrows were in locations with lower vegetation density than random points However lizards moving between burrows in spring showed a tendency to choose burrows with relatively more surrounding vegetation. Our initial hypothesis that lizards would prefer burrows with an intermediate level of grazing that produced some reduction of vegetation cover was not completely supported, probably because lizards often choose burrows early in spring when grasslands have denser vegetation cover, and then tend to remain in the same burrow as grazing or seasonal drying reduces vegetation cover. Changes in vegetation do not seem to induce lizard movement.

The impact of sheep grazing on the fecundity and timing of reproduction in the endangered pygmy bluetongue lizard, Tiliqua adelaidensis

The endangered pygmy bluetongue lizard (Tiliqua adelaidensis) is found only in a few remaining patches of South Australian native grassland, most of which are used for live stock grazing. The lizards occupy spider burrows, they mate in October-November and females produce litters of one to four live born neonates in mid-January-mid-March. In this study we use ultrasound scans of females and observations of neonates in their maternal burrows to investigate how grazing affects the fecundity of the pygmy bluetongue lizard. We predicted that lizards in moderately grazed paddocks would have a higher reproductive output than lizards in hard grazed paddocks. Ultrasound scans indicated that this hypothesis was correct by showing a higher mean number of yolk sacs in females from moderately than from hard grazed paddocks. Females from moderately grazed paddocks also gave birth significantly earlier than females in hard grazed paddocks. The higher number of yolk sacs did not result in a significantly higher number of neonates observed in the burrows, which indicates that the weekly burrow observations used in this study may underestimate true fecundity. Understanding how grazing affects the fecundity of the pygmy bluetongue lizard is essential to the future management of this endangered species. This is not only because grazing is used to manage the habitat of all currently known lizard populations, but also because successful reproduction will be needed in those populations to supply the “surplus” individuals predicted to be essential for relocation programs to ensure the survival of the species.

A nose for lizards; can a detection dog locate the endangered pygmy bluetongue lizard (Tiliqua adelaidensis)?

ABSTRACTEnvironmental detection dogs have been used in various research and conservation projects. By detecting scent, dogs are capable of finding animals or scats that are virtually undetectable to humans. The endangered pygmy bluetongue lizard (Tiliqua adelaidensis) is endemic to heavily fragmented patches of native grassland in the mid-north region of South Australia. The lizards live in spider burrows with entrance diameters of 10–20 mm, which makes them difficult to find. This study presents the first data showing that a dog can detect pygmy bluetongue lizards. The dog showed the ability to distinguish between pygmy bluetongue lizard scent and the scent of sleepy lizard (Tiliqua rugosa) and bearded dragon (Pogona barbata). The dog also found more than 30 occupied lizard burrows in the field. Up until now surveys of this endangered lizard have relied on human visual detection of burrows, which is a very labour-intensive process. Although the climate and the ecology of the lizards pose a challenge to detection dogs, this study showed that their use in surveys of pygmy bluetongue lizards could potentially increase efficiency and accuracy, while lowering the cost and the workload.

Impact of foxes digging for the pygmy bluetongue lizard (Tiliqua adelaidensis)

ABSTRACTThe endangered pygmy bluetongue lizard (Tiliqua adelaidensis) is endemic to heavily fragmented patches of native grassland in the mid-north region of South Australia. The lizards live in spider burrows, and suitable burrows can be a limiting factor to local populations. The invasive red fox (Vulpes vulpes) is a likely predator of the lizards. No previous research has focussed on the effects of foxes on pygmy bluetongue lizards. This article presents observations from three sampling rounds in a single lizard activity season. During each round, burrows were located and lizard presence or absence, fox digging and burrow condition were recorded. Out of 256 monitored lizard burrows, 12 were dug out by foxes. The data show that foxes actively seek to prey on pygmy bluetongue lizards. In several cases, the fox gave up before reaching the lizard. Dug out burrows were quickly abandoned by the surviving lizards and became filled in, reducing the supply of suitable burrows for the population. These data highlight the need for fox management around pygmy bluetongue lizard populations, especially if future management of the species involves relocation, as small newly established populations could be vulnerable to fox predation and secondary effects of burrow destruction.

Ontogenetic changes in head scale symmetry in the pygmy bluetongue lizard

ABSTRACTFluctuating asymmetry (FA, small and random deviations from perfect symmetry in otherwise bilaterally symmetrical traits) has been used as a monitoring tool for species at risk. Differences in the levels of FA in a trait are attributed to the different levels of environmental or genetic stressors during the developmental phase of an organism. In this study, we used a symmetry index (SI) in the head scales of the endangered pygmy bluetongue lizard, Tiliqua adelaidensis, to investigate the relationship between the SI and jaw width (JW) (as an indirect measure of fitness) among lizards from different age classes (neonate, subadult and adult) to shed light on the ontogeny of symmetry. Also, we explored changes in the levels of symmetry among different age classes to determine possible selection processes. Our findings showed that there was a positive relationship between the SI and JW in neonates (individuals with larger jaws were more symmetric) whereas the trend was reversed in adults (individuals with larger jaws were less symmetric). The relationship was not significant in subadults. This confirms that a transition happened during the growth of lizards. We suggest this resulted from adults allocating more resources to the growth rather than symmetry of head scales. We found no significant differences in the mean SI between adults and neonates, although subadults showed significantly higher values of the SI. This study has revealed some valuable insights into ontogenetic changes in symmetry of head scales in pygmy bluetongue lizards, but it did not provide any evidence that survival from neonate to adult is influenced by head scale symmetry.

The impact of sheep grazing on the depth of spider burrows and of burrows selected by the pygmy bluetongue lizard (Tiliqua adelaidensis)

Context Grazing by domestic stock can potentially influence ecosystems positively or negatively, depending on the grazing regime and intensity. The pygmy bluetongue lizard (Tiliqua adelaidensis) is an endangered species, restricted to fragmented grasslands in the Mid North region of South Australia, predominantly grazed by sheep. These lizards refuge in vertical burrows. They do not dig their own burrows, instead relying on co-existing spiders for this essential resource. Aims We investigated how sheep grazing influenced spider burrows, and predicted the following: that grazing sheep might trample and destroy shallow burrows; that burrows in grazed habitat with less vegetative cover would have higher temperatures in summer; and that, by way of compensation, spiders would dig deeper burrows in grazed habitat. Methods We monitored 12 30m×30m plots monthly, over two austral spring/summer periods (September–March 2012–14). We recorded the number, depth and occupant of all spider burrows in those plots in each survey. We also measured temperatures inside artificial burrows in grazed and ungrazed habitat over a 3-day period in September 2014. Key results Mean burrow depth increased with grazing. This was not because individual burrows became deeper, but because the shallowest burrows were lost where there were sheep. Burrows were significantly hotter in grazed habitat, but lizards consistently chose deeper, cooler burrows. In the subset of burrows that were occupied by lizards, there was no difference in depth between grazed and ungrazed treatments. We detected no difference in spider digging activity between grazed and ungrazed plots. Conclusions Sheep grazing can destroy shallow burrows, probably through trampling, and because sheep produce burrow filling debris. However, grazing did not affect deeper burrows occupied by pygmy bluetongue lizards. Implications This short study indicated that moderate levels of grazing have low impact on deeper burrows suitable for pygmy bluetongue lizards and for lizard persistence. It explains how sheep and lizards have co-occurred for so long, but leaves open the question of how the loss of shallow burrows affects populations of the burrow-digging spiders that are an essential component of the lizard environment.

Winter durability of pygmy bluetongue lizard burrows is higher for occupied than for unoccupied burrows and for those in less-grazed neighbourhoods

Context Many ectothermic animals survive winter by hibernating, either buried or in burrows. During their hibernation these animals are vulnerable to changes in soil structure and temperature caused by the activity of grazing mammals. This may be a particular risk to ectotherms living in native grassland, as this habitat is often used for livestock grazing. The endangered pygmy bluetongue lizard lives in burrows, in fragments of native grassland in South Australia, and these burrows are likely to be affected by sheep grazing during the lizards’ hibernation. Aims The current study aimed to determine the following effects on the persistence of burrows suitable to the pygmy bluetongue lizard: different levels of grazing, winter vegetation cover, burrow entrance size and whether a lizard was overwintering in the burrow. Methods During two winters, we applied different grazing treatments to six experimental paddocks and determined whether suitable lizard burrows located in autumn were still suitable to lizards in the following spring. For each burrow, we recorded whether a lizard was overwintering, the burrow entrance diameter and the vegetation cover around the burrow during the winter. Key results Increased grazing pressure led to decreased persistence of lizard burrows. We also found that burrows with an overwintering lizard had a greater chance of persisting, but found no direct effect of winter vegetation cover or entrance diameter. Conclusions The results show that although pygmy bluetongue lizards may be able to stabilise their own burrows, the more intense the grazing the lower the chance of lizard burrow persistence. Implications Management of sheep grazing is an important component in future conservation of the endangered pygmy bluetongue lizard. Grazing on grassland with a lizard population should be kept at a moderate level and hard grazing should be avoided.

Scatting behaviour of the pygmy bluetongue lizard

We used video recordings of 29 pygmy bluetongue lizards for ten days of each month during their spring and summer activity season to observe scatting behaviour. This was possible because resident lizards rarely moved from their single entrance burrows. We used these observations to ask questions about social communication that might be relevant to conservation of this endangered species. We found lizards produced more scats in the middle of the day than earlier or later in the day, and more scats in the spring and early summer than later in the summer. Lizards moved an average of 68.54 ± 0.09 cm from their burrow entrance to deposit scats, taking an average of 2.4 min per defecation trip. They tended to use the same path direction for most defecation trips, but used more different directions if there were more close neighbours, strongly supporting a hypothesis that scats mark burrow ownership. The results suggested that conservation managers might reduce stress for relocated lizards by removing scat piles in the early stages of settlement.

A thirsty little lizard: drinking by the pygmy bluetongue lizard

ABSTRACTThe pygmy bluetongue lizard (Tiliqua adelaidensis) is an endangered scincid lizard, endemic to the Mid North region of South Australia, where it occupies heavily fragmented patches of native grassland. Pygmy bluetongue lizards live in spider burrows and rarely venture far from their burrows. This limits their access to free standing water, and it was previously unknown whether lizards acquired all the water they needed from their food, or whether they could access an alternative source of water. This paper presents 27 observations of lizards drinking either from drops of morning dew or from rain drops accumulated on vegetation close to their burrow entrances. These observations suggest that pygmy bluetongue lizards can supplement their water requirements independent of free standing water sources, like streams or ponds, if there is vegetation that can collect dew and rain close to burrow entrances. Vegetation that can hold water droplets for a short time provides flexibility for the lizards in maintaining their water budgets. The water collecting function of vegetation should be included as a factor in short-term management decisions about the level of grazing in the lizard’s habitat. In the longer term, the benefits of having plants that can accumulate water drops will need to be considered if suitable relocation sites are to be found.

Interactions between pygmy bluetongue lizards and co-existing species

This article describes observations of interactions between endangered pygmy bluetongue lizards (Tiliquaadelaidensis) and other species that co-occur in their native grassland habitat in the mid-north region of South Australia. The lizard lives in spider burrows, and rarely moves away from the burrow entrance. We viewed over 16,000 h of video recording of occupied pygmy bluetongue lizard burrows, taken over five 10-day periods throughout one complete lizard activity season, and documented all cases in which these endangered lizards interacted with co-existing species. We found that these interactions were infrequent. We observed potential competition over burrow resources with lycosid spiders (Lycosaspp), centipedes, and a house mouse, and potential competition over invertebrate prey with a predatory wasp. We also observed unsuccessful predation attempts on lizards in burrows by ravens and brown snakes. We suggest that conservation management might have proceeded effectively without this information, but that it provides useful background information for informed decision making.

Variation in size and condition of neonate pygmy bluetongue lizards, Tiliqua adelaidensis

Phenotypic variation among offspring of individual animals is an important life-history trait. In viviparous lizards, it could result from genetic variation of individuals and also differences in environments experienced by mothers during gestation. We investigated variation in phenotype and survival of neonate pygmy bluetongue lizards, Tiliqua adelaidensis, over three sampling years. We explored changes in body condition, using body size residuals as an index, and body size (snout-vent length (SVL) and mass) of neonates. For litters that were captured with their mothers, we hypothesised that body condition and size of offspring are influenced by the condition and size of their mothers, the presence of mothers in the burrow and litter size. We found that there were significant variations in body condition and mass of neonates among years. There was no significant relationship between neonate body condition, mass and SVL and post-partum body condition of their mothers. Results revealed that females with higher SVL produced larger litters. None of the analyses showed any effect of mother’s presence on neonate body condition, SVL or mass. Neither was there any effect of observed litter size on these parameters. Our findings have important conservation implications for this endangered species, given that the aim of conservation managers is to encourage conditions that promote optimum body condition and fitness in offspring in order to maximise their survival in fragmented habitats.

The impact of sheep grazing on burrows for pygmy bluetongue lizards and on burrow digging spiders

AbstractGrazing by domestic stock has altered and degraded natural grassland ecosystems worldwide, directly and indirectly impacting the endemic plant and animal species occupying those grasslands. The pygmy bluetongue lizard Tiliqua adelaidensis is an endangered species, restricted now to fragments of native grassland habitat in South Australia, which are predominantly grazed by sheep. These lizards exclusively occupy burrows dug by spiders, and use them as refuges, basking sites and ambush points. They do not dig their own burrows and rely on coexisting spiders for this essential resource. We asked how sheep grazing influences construction and persistence of spider burrows by comparing burrow dynamics in adjacent grazed and ungrazed grassland habitats. In ungrazed plots, spider burrows increased over one spring and summer period, particularly after a summer rain event that softened the soil. In grazed plots, more existing burrows were destroyed, presumably by sheep trampling, and fewer new burrows were constructed, leading to a net loss in burrow numbers over the same period. However, in this short study, grazing did not affect the number of pygmy bluetongue lizards or the number of lycosid spiders. Burrows that were lost tended to be shallower and to have smaller diameter entrances than those that were retained, suggesting that the best burrows for lizard refuges were more likely to persist despite sheep activity. However, heavy grazing may have negative impacts on both lizards and spiders, resulting from a reduction in available burrows and in spider digging behaviour.

Long and short term residence in refuge burrows by endangered pygmy bluetongue lizards

The pygmy bluetongue lizard (Tiliqua adelaidensis) is an endangered species which is restricted to native grassland remnants in South Australia. Individuals live in vertical burrows with a single entrance from which they ambush invertebrate prey. We monitored marked burrows over two entire spring-summer seasons, the period when the lizards are active, and found that the population contained a mixture of dispersers that remained in a burrow briefly, and residents that occupy a burrow for the entire study period. There were more females than males among the residents and most of the burrow abandonment happened in the early spring, the time when male lizards probably move around to seek matings. Our study described burrow occupancy dynamics, and will assist the conservation management of this endangered species.