Stephanie S. Godfrey

Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii

Gidgee skinks (Egernia stokesii) form large social aggregations in rocky outcrops across the Flinders Ranges in South Australia. Group members share refuges (rock crevices), which may promote parasite transmission. We measured connectivity of individuals in networks constructed from patterns of common crevice use and observed patterns of parasitism by three blood parasites (Hemolivia, Schellackia and Plasmodium) and an ectoparasitic tick (Amblyomma vikirri). Data came from a 1-year mark-recapture study of four populations. Transmission networks were constructed to represent possible transmission pathways among lizards. Two lizards that used the same refuge within an estimated transmission period were considered connected in the transmission network. An edge was placed between them, directed towards the individual that occupied the crevice last. Social networks, a sub-set of same-day only associations, were small and highly fragmented compared with transmission networks, suggesting that non-synchronous crevice use leads to more transmission opportunities than direct social association. In transmission networks, lizards infested by ticks were connected to more other tick-infested lizards than uninfected lizards. Lizards infected by ticks and carrying multiple blood parasite infections were in more connected positions in the network than lizards without ticks or with one or no blood parasites. Our findings suggest higher levels of network connectivity may increase the risk of becoming infected or that parasites influence lizard behaviour and consequently their position in the network.

Networks and the ecology of parasite transmission: A framework for wildlife parasitology.

Graphical abstract

Using social networks to deduce whether residents or dispersers spread parasites in a lizard population.

1. Heterogeneity of host behaviour can play an important role in the spread of parasites and pathogens around wildlife populations. Social networks have previously been suggested to represent transmission pathways within a population, but where the dynamics of host-parasite interactions are difficult to observe, networks may also be used to provide insights into transmission processes. 2. Pygmy bluetongue lizards, Tiliqua adelaidensis, occupy individual territories, live exclusively in burrows constructed by spiders in Australian native grasslands and are hosts to a tick, Bothriocroton hydrosauri, and a nematode, Pharyngodon wandillahensis. 3. On five monthly occasions, the locations of all individual lizards in three study plots were used to construct weighted, undirected networks based on proximity of adjacent burrows. 4. The networks were used to explore alternative hypotheses about the spread of each parasite through the population: that stable population members that remained in the same burrow over the study period played a major role in influencing the pattern of infection or that dispersing individuals played a more significant role. 5. For ticks, host individuals that were infected were more connected in the network than uninfected hosts and this relationship remained significant for connections to residents in the population, but not for connections to dispersers. 6. For nematodes, infected and uninfected hosts did not differ in their overall strength of connection in the network, but infected hosts were more connected to dispersers than were uninfected hosts, suggesting that lizards moving across the population are the major agents for the transmission of nematodes. 7. This study shows how network analyses can provide new insights into alternative pathways of parasite spread in wildlife populations, where it is difficult to make direct observations of transmission-related behaviours.

Social network structure and parasite infection patterns in a territorial reptile, the tuatara (Sphenodon punctatus)

We investigated whether the parasite load of an individual could be predicted by its position in a social network. Specifically, we derived social networks in a solitary, territorial reptile (the tuatara, Sphenodon punctatus), with links based on the sharing of space, not necessarily synchronously, in overlapping territories. Tuatara are infected by ectoparasitic ticks (Amblyomma sphenodonti), mites (Neotrombicula spp.) and a blood parasite (Hepatozoon tuatarae) which is transmitted by the tick. We recorded the location of individual tuatara in two study plots twice daily during the mating season (March) in 2years (2006 and 2007) on Stephens Island, New Zealand. We constructed weighted, directed networks to represent pathways for parasite transmission, where nodes represented individual tuatara and edges connecting the nodes represented the extent of territory overlap among each pair of individuals. We considered a network-based hypothesis which predicted that the in-strength of individuals (the sum of edge weights directed towards a node) in the derived network would be positively related to their parasite load. Alternatively, if the derived social network did not reflect actual parasite transmission, we predicted other factors such as host sex, size or territory size may better explain variation in parasite infection patterns. We found clear positive relationships between the in-strength of tuatara and their tick loads, and infection patterns with tick-borne blood parasites. In particular, the extent that individuals were connected to males in the network consistently predicted tick loads of tuatara. However, mite loads of tuatara were significantly related to host sex, body size and territory size, and showed little association with network measures. The results suggest that the pathway of transmission of parasites through a population will depend on the transmission mechanism of the parasite, but that social networks provide a powerful predictive tool for some parasites.

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.

Transmission mode and distribution of parasites among groups of the social lizard Egernia stokesii

We explored patterns of infection of three apicomplexan blood parasites with different transmission mechanisms in 46 social groups across seven populations of the Australian lizard, Egernia stokesii. There was higher aggregation of infections within social groups for Hemolivia, transmitted by ticks, and Schellackia, either tick-transmitted or directly transmitted from mother to offspring, than for Plasmodium, with more mobile dipteran vectors. Prevalence was not related to group size, proximity to other groups or spatial overlap with adjacent groups for any of the parasites. However, for Hemolivia, groups with higher levels of relatedness among adults had higher parasite prevalence. Living in social groups leads to higher risk of infection for parasites with low transmission mobility. An unanswered question is why so few lizard species tolerate these risks to form stable social aggregations.

Morphological polymorphism of Trypanosoma copemani and description of the genetically diverse T. vegrandis sp. nov. from the critically endangered Australian potoroid, the brush-tailed bettong (Bettongia penicillata (Gray, 1837))

BackgroundThe trypanosome diversity of the Brush-tailed Bettong (Bettongia penicillata), known locally as the woylie, has been further investigated. At a species level, woylies are critically endangered and have declined by 90% since 1999. The predation of individuals made more vulnerable by disease is thought to be the primary cause of this decline, but remains to be proven.MethodsWoylies were sampled from three locations in southern Western Australia. Blood samples were collected and analysed using fluorescence in situ hybridization, conventional staining techniques and microscopy. Molecular techniques were also used to confirm morphological observations.ResultsThe trypanosomes in the blood of woylies were grouped into three morphologically distinct trypomastigote forms, encompassing two separate species. The larger of the two species, Trypanosoma copemani exhibited polymorphic trypomastigote forms, with morphological phenotypes being distinguishable, primarily by the distance between the kinetoplast and nucleus. The second trypanosome species was only 20% of the length of T. copemani and is believed to be one of the smallest recorded trypanosome species from mammals. No morphological polymorphism was identified for this genetically diverse second species. We described the trypomastigote morphology of this new, smaller species from the peripheral blood of the woylie and proposed the name T. vegrandis sp. nov. Temporal results indicate that during T. copemani Phenotype 1 infections, the blood forms remain numerous and are continuously detectable by molecular methodology. In contrast, the trypomastigote forms of T. copemani Phenotype 2 appear to decrease in prevalence in the blood to below molecular detectable levels.ConclusionsHere we report for the first time on the morphological diversity of trypanosomes infecting the woylie and provide the first visual evidence of a mixed infection of both T. vegrandis sp. nov and T. copemani. We also provide supporting evidence that over time, the intracellular T. copemani Phenotype 2 may become localised in the tissues of woylies as the infection progresses from the active acute to chronic phase. As evidence grows, further research will be necessary to investigate whether the morphologically diverse trypanosomes of woylies have impacted on the health of their hosts during recent population declines.

Trypanosomes of Australian mammals: A review

Approximately 306 species of terrestrial and arboreal mammals are known to have inhabited the mainland and coastal islands of Australia at the time of European settlement in 1788. The exotic Trypanosoma lewisi was the first mammalian trypanosome identified in Australia in 1888, while the first native species, Trypanosoma pteropi, was taxonomically described in 1913. Since these discoveries, about 22% of the indigenous mammalian fauna have been examined during the surveillance of trypanosome biodiversity in Australia, including 46 species of marsupials, 9 rodents, 9 bats and both monotremes. Of those mammals examined, trypanosomes have been identified from 28 host species, with eight native species of Trypanosoma taxonomically described. These native trypanosomes include T. pteropi, Trypanosoma thylacis, Trypanosoma hipposideri, Trypanosoma binneyi, Trypanosoma irwini, Trypanosoma copemani, Trypanosoma gilletti and Trypanosoma vegrandis. Exotic trypanosomes have also been identified from the introduced mammalian fauna of Australia, and include T. lewisi, Trypanosoma melophagium, Trypanosoma theileri, Trypanosoma nabiasi and Trypanosoma evansi. Fortunately, T. evansi was eradicated soon after its introduction and did not establish in Australia. Of these exotic trypanosomes, T. lewisi is the sole representative that has been reported from indigenous Australian mammals; morphological forms were recorded from two indigenous species of rodents (Hydromys chrysogaster and Rattus fuscipes). Numerous Australian marsupial species are potentially at risk from the native T. copemani, which may be chronically pathogenic, while marsupials, rodents and monotremes appear at risk from exotic species, including T. lewisi, Trypanosoma cruzi and T. evansi. This comprehensive review of trypanosome biodiversity in Australia highlights the negative impact of these parasites upon their mammalian hosts, as well as the threatening biosecurity concerns.

Temporal and spatial dynamics of trypanosomes infecting the brush-tailed bettong (Bettongia penicillata): a cautionary note of disease-induced population decline

BackgroundThe brush-tailed bettong or woylie (Bettongia penicillata) is on the brink of extinction. Its numbers have declined by 90% since 1999, with their current distribution occupying less than 1% of their former Australian range. Woylies are known to be infected with three different trypanosomes (Trypanosoma vegrandis, Trypanosoma copemani and Trypanosoma sp. H25) and two different strains of T. copemani that vary in virulence. However, the role that these haemoparasites have played during the recent decline of their host is unclear and is part of ongoing investigation.MethodsWoylies were sampled from five locations in southern Western Australia, including two neighbouring indigenous populations, two enclosed (fenced) populations and a captive colony. PCR was used to individually identify the three different trypanosomes from blood and tissues of the host, and to investigate the temporal and spatial dynamics of trypanosome infections.ResultsThe spatial pattern of trypanosome infection varied among the five study sites, with a greater proportion of woylies from the Perup indigenous population being infected with T. copemani than from the neighbouring Kingston indigenous population. For an established infection, T. copemani detection was temporally inconsistent. The more virulent strain of T. copemani appeared to regress at a faster rate than the less virulent strain, with the infection possibly transitioning from the acute to chronic phase. Interspecific competition may also exist between T. copemani and T. vegrandis, where an existing T. vegrandis infection may moderate the sequential establishment of the more virulent T. copemani.ConclusionIn this study, we provide a possible temporal connection implicating T. copemani as the disease agent linked with the recent decline of the Kingston indigenous woylie population within the Upper Warren region of Western Australia. The chronic association of trypanosomes with the internal organs of its host may be potentially pathogenic and adversely affect their long term fitness and coordination, making the woylie more susceptible to predation.

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.