Christopher Michael Bull

Consistent social structure within aggregations of the Australian lizard, Egernia stokesii across seven disconnected rocky outcrops

The Australian skink lizard Egernia stokesii lives in aggregations of up to 17 individuals. Previously, at one site, these aggregations have been shown to comprise paired unrelated individuals and several cohorts of their young. To investigate whether social structuring in this species is a response to ecological conditions or is phylogenetically constrained, we sampled social aggregations of E. stokesii from seven geographically adjacent rocky outcrops (including the site previously studied) that differ in the availability of homesite crevices. Analysis of genotypes from ten microsatellite loci indicate that social structures were similar at all sites and were comparable with that of the previous study. Over all sites highly significant positive relationships were observed between the number of crevices at a site and both the number of lizards and the number of social groups. Social structure in this species seems to be phylogenetically constrained, at least in relation to the abundance of potential homesite crevices.

When the going gets tough: behavioural type-dependent space use in the sleepy lizard changes as the season dries.

Understanding space use remains a major challenge for animal ecology, with implications for species interactions, disease spread, and conservation. Behavioural type (BT) may shape the space use of individuals within animal populations. Bolder or more aggressive individuals tend to be more exploratory and disperse further. Yet, to date we have limited knowledge on how space use other than dispersal depends on BT. To address this question we studied BT-dependent space-use patterns of sleepy lizards (Tiliqua rugosa) in southern Australia. We combined high-resolution global positioning system (GPS) tracking of 72 free-ranging lizards with repeated behavioural assays, and with a survey of the spatial distributions of their food and refuge resources. Bayesian generalized linear mixed models (GLMM) showed that lizards responded to the spatial distribution of resources at the neighbourhood scale and to the intensity of space use by other conspecifics (showing apparent conspecific avoidance). BT (especially aggressiveness) affected space use by lizards and their response to ecological and social factors, in a seasonally dependent manner. Many of these effects and interactions were stronger later in the season when food became scarce and environmental conditions got tougher. For example, refuge and food availability became more important later in the season and unaggressive lizards were more responsive to these predictors. These findings highlight a commonly overlooked source of heterogeneity in animal space use and improve our mechanistic understanding of processes leading to behaviourally driven disease dynamics and social structure.

Molecular genetic data provide support for a model of transmission dynamics in an Australian reptile tick, Bothriocroton hydrosauri

Bothriocroton hydrosauri is a three‐host ixodid tick that infests large reptiles in southeastern Australia, where its most common host is a large scincid lizard Tiliqua rugosa. Based on previous ecological and behavioural studies of this system, we propose a ‘ripple’ model of tick population dynamics, where only a few female ticks succeed in producing surviving offspring. These females then are the centres of ripples of their progeny spreading into the broader landscape. The model predicts higher relatedness among larvae than among nymphs or adults on a host, and significant spatial autocorrelation in larvae extending further than for the later life stages. The model also predicts that adult ticks are likely to encounter related partners and that this will generate inbreeding within the population. We tested those predictions using nine polymorphic microsatellite loci on a sample of 848 ticks (464 larvae, 140 nymphs and 244 adults) collected from 98 lizard hosts from near Bundey Bore Station in South Australia. Our data support the predictions and indicate that the dynamics of transmission among hosts play an important role in parasite population structure.

The use of scats as social signals in a solitary, endangered scincid lizard, Tiliqua adelaidensis

Context The deliberate accumulation of faeces or scats in one location is a common behaviour used for social signalling. The endangered pygmy bluetongue lizard, Tiliqua adelaidensis, is a solitary-living species that appears to use scats as social signals. Previous studies have found that these lizards approach burrows more cautiously if there is a conspecific scat present and behave differently to scats from male and female conspecifics, indicating that these lizards can recognise scat-based conspecific cues. For endangered species, understanding how an animal uses and responds to chemical cues has the potential to become a powerful tool in conservation management. Aims To investigate whether these solitary lizards might be using scats as social signals by testing whether scats were being deposited in a non-random pattern designed to maximise their exposure to the nearest neighbour conspecifics. Method In the present study, we investigated the spatial pattern of scatting behaviour by pygmy bluetongue lizards in the field. Results Scats were consistently deposited in one direction that was significantly aligned with the nearest occupied burrow of a neighbouring lizard. The same deposition sites were used when previous scats were either destroyed by rain, or experimentally moved to a different location. Male lizards deposited scats significantly closer to their own burrows when neighbours were closer. Key conclusions The results were consistent with the lizards using scats to advertise their presence and status. The scat-deposition patterns observed in the present study suggest that scats are used as an olfactory signal associated with social organisation of pygmy bluetongue lizards. Implications Current plans for the conservation management of this endangered species include translocations. By understanding how these lizards respond to, and use chemical cues, we may be able to use this knowledge to aid in translocation programs, e.g. by pre-establishing territories for individuals before they are introduced into the population.

Optimising the design of artificial refuges for the Australian skink, Egernia stokesii

Western subspecies of the Australian skink Egernia stokesii are considered endangered and translocation to unoccupied areas of suitable habitat has been proposed as a conservation strategy. We investigated the internal structure of artificial refuges that might induce translocated lizards to remain at the site of release. In a laboratory environment, individual lizards were offered choices of alternative structures as refuges. They preferred deeper and narrower refuge structures, with a single entrance rather than two entrances. They showed a slight tendency to avoid PVC structures when plywood or brick paving alternatives were available. Soft sand or hard brick substrate were equally accepted. The results suggest that the use of brick pavers may be a practical management strategy to provide extra refuges for the lizards, but further trials are needed with a greater range of temperatures that are representative of field conditions.

Fine-scale spatial structuring as an inbreeding avoidance mechanism in the social skink Egernia stokesii

Abstract. Egernia stokesii is a monogamous and group-living species of Australian scincid lizard. We used genotype data from 10 microsatellite loci to examine evidence for sex-biased dispersal and kin-based discrimination as mechanisms for inbreeding avoidance of E. stokesii within seven rocky outcrops in the southern Flinders Ranges of South Australia. We also examined the relatedness of individuals observed using the same crevice within groups. We found no evidence for sex-biased dispersal at these sites, but found that adult lizards of the opposite sex observed using the same crevice were less related to each other than expected by chance. Our results suggest a behavioural mechanism for minimising inbreeding in large related aggregations of this species.

Piles of scats for piles of DNA: deriving DNA of lizards from their faeces

Abstract. Non-invasive genetic sampling using scats has a well established role in conservation biology, but has rarely been applied to reptiles. Using scats from captive and wild Egernia stokesii (Squamata, Scincidae) we evaluated two storage and six DNA-extraction methods and the reliability of subsequent genotype and sequence data. Accurate genotype and sequence data were obtained from frozen and dried captive lizard scat DNA extracted using a QIAamp® DNA Stool Mini Kit and a modified Gentra® Puregene® method, but success rates were reduced for wild lizard scats. Wild E. stokesii eat more plants than their captive counterparts, possibly resulting in scat DNA extracts containing plant compounds that inhibit PCR-amplifications. Notably, reliable genotypes and sequences were obtained from wild E. stokesii scat DNA extracted using a Qiagen DNeasy® Plant Mini Kit, a method designed to remove plant inhibitory compounds. Results highlight the opportunity for using scat-derived DNA in lizard studies, particularly for species that deposit scats in piles.

MHC genotyping from next-generation sequencing: detailed methodology for the gidgee skink, Egernia stokesii

ABSTRACT Next-generation sequencing has revolutionised molecular ecology. Its key advantages are a more accurate representation of genetic variation made possible by the generation of large volumes of data, more quickly and at a lower price per sequence than traditional sequencing methods. Yet these benefits come with a cost. For example, next-generation sequencing is error prone and requires increased quality control compared with traditional methods. Problems associated with next-generation sequencing may be exacerbated when sequencing gene complexes such as the major histocompatibility complex (MHC). Although not eliminated, significant progress has been made in addressing some of those problems and there is an increasing literature utilising this technology for studies of the MHC. However, what is generally lacking is detailed documentation of the methods used, and clear reasoning, for each step. Here we document detailed methodology, using an Australian lizard, Egernia stokesii, as a case study, with explanations, for MHC amplification, sequencing and allele identification. This work provides molecular ecologists with a comprehensive guide to follow, particularly when first employing next-generation sequencing techniques similar to those used here. In addition, the E. stokesii MHC genotypes derived from this work provide foundation data for future investigations of the influence of social structure on the MHC.

Dynamics of a temperate grassland reptile community in the mid-north of South Australia

Abstract Temperate native grasslands are listed as a critically endangered ecological community in South Australia, yet very little is known about the associated faunal communities. This study aims to provide information on the temporal dynamics of a native grassland reptile community in the mid-north of South Australia. During the study we made 335 reptile captures in pitfall traps, of 248 different individuals, from 13 species, representing five families. These data were used to investigate seasonal trends in trapping rate, age demographics and movement of individuals from marked recaptures. The results of the study provide baseline information on species assemblages that might be used in the recovery and management of the remaining fragments of temperate native grasslands and the endangered pygmy bluetongue lizard that relies on those fragments for its persistence.

Larger lizards live longer in the group-living Egernia stokesii

Abstract. Animal space use has implications for gene flow, disease dynamics, mating systems and the evolution of sociality. Given recent attention to sociality in reptiles, lizards are an important group for expanding our understanding of animal space use. Lizard space use is commonly investigated within one population over a short period and limited attention has been given to potential predictors of site fidelity. This study evaluated site fidelity in three populations of group-living Egernia stokesii (gidgee skink) between two field surveys separated by almost a decade. Of 43 recaptured lizards, 28 (65%) occupied their original space, and 15 (36%) of those shared their space with the same other lizard or lizards in both surveys. This confirmed long-term site and social bond fidelity in E. stokesii. We found that larger lizards were more likely to be recaptured. Neither body size, individual genetic heterozygosity, nor the availability of refuges strongly predicted whether lizards were recaptured in the same or a different place. The reasons why some lizards stayed in the same space while others moved are yet to be resolved.