Native Australian Rodent Research Articles

Maternal genetic and non-genetic effects on the development of exploration and anxiety-like behaviours in a native Australian rodent, the fawn-footed mosaic-tailed rat Melomys cervinipes

Abstract Personality in non-human animals has been a popular area of research; however, it is still unknown how genetic and non-genetic factors influence the development of personality in many species. Therefore, we investigated how maternal genetic and non-genetic effects influenced adult offspring personality (exploration and anxiety) in the fawn-footed mosaic-tailed rat Melomys cervinipes. We first measured the amount of maternal care mothers provided to their offspring. Later, we assessed mothers and adult offspring over two testing sessions for exploratory behaviour using open field and novel object tests, and anxiety behaviour in a light/dark test. We calculated repeatability of behaviours and used parent–offspring regressions to assess heritability of behaviours. No measure of maternal care significantly influenced offspring personality. However, exploration of new spaces was constrained by maternal genetic effects. In contrast, anxiety and exploration of novel objects was more flexible, suggesting these behaviours may be more influenced by an individual’s experiences during development.

The consistency of exploration behaviours across life stages in a native Australian rodent, the fawn-footed mosaic-tailed rat Melomys cervinipes.

Many species show inter-individual variation in exploratory behaviours that are consistent over time, reflecting a personality. Differences in exploration can affect how individuals acquire resources and use their environment. However, few studies have considered whether exploratory behaviours are consistent across developmental life stages, such as when individuals disperse out the natal territory or when they become sexually mature. We therefore investigated the consistency of exploration behaviours towards a novel object and novel environment in a native Australian rodent, the fawn-footed mosaic-tailed rat Melomys cervinipes across development. Individuals were tested in an open field test and novel object test for five trials across four different life stages (pre-weaning, recently weaned, independent juvenile, sexually mature adult). We found that individual mosaic-tailed rats were consistent in their exploration of novel objects over these life stages, as these behaviours were repeatable. However, how individuals explored novel environments was not repeatable and changed across development, with exploration peaking during the independent juvenile stage. These results suggest that the way an individual interacts with novel objects may be somewhat constrained by genetic or epigenetic effects early in development, whereas spatial exploration could be more flexible to facilitate developmental shifts, such as dispersal. The life stage of an animal should therefore be taken into consideration when assessing personality in different species.

The effects of antibiotics and illness on gut microbial composition in the fawn-footed mosaic-tailed rat (Melomys cervinipes).

The gut microbiota are critical for maintaining the health and physiological function of individuals. However, illness and treatment with antibiotics can disrupt bacterial community composition, the consequences of which are largely unknown in wild animals. In this study, we described and quantified the changes in bacterial community composition in response to illness and treatment with antibiotics in a native Australian rodent, the fawn-footed mosaic-tailed rat (Melomys cervinipes). We collected faecal samples during an undiagnosed illness outbreak in a captive colony of animals, and again at least one year later, and quantified the microbiome at each time point using 16s ribosomal rRNA gene sequencing. Gut bacterial composition was quantified at different taxonomic levels, up to family. Gut bacterial composition changed between time periods, indicating that illness, treatment with antibiotics, or a combination affects bacterial communities. While some bacterial groups increased in abundance, others decreased, suggesting differential effects and possible co-adapted and synergistic interactions. Our findings provide a greater understanding of the dynamic nature of the gut microbiome of a native Australian rodent species and provides insights into the management and ethical well-being of animals kept under captive conditions.

Comparative tongue anatomy of the rakali (Hydromys chrysogaster) and greater stick-nest rat (Leporillus conditor) (Rodentia; Muridae)

For many mammals, the tongue provides an important functional interface with the environment through roles including manipulating, ingesting, and mechanically processing food items. As such, the adaptations of the tongue reflect different physical properties of an animal’s diet. We sought to investigate whether adaptations of the tongue are apparent in two native Australian rodents that have divergent dietary niches: the semiaquatic and mixed feeding rakali (Hydromys chrysogaster) and the arid dwelling, herbivorous stick-nest rat (Leporillus conditor). Both species retained many lingual features typical of rodents. A notable difference was a large, annular pad surrounding the single circumvallate papilla in H. chrysogaster, suggesting an enhanced gustatory function, which would be consistent with adaptation to a semiaquatic, mixed diet. In contrast, L. conditor appeared to have reduced gustatory sensitivity and mechanical dexterity, consistent with crushing their preferred succulent plant forage and manipulating sticks for nest building. The descriptions provide a novel view of the evolution of soft tissues within Australian endemic rodents.

Both age and experience are important for successful problem solving in juvenile fawn-footed mosaic-tailed rats Melomys cervinipes.

Problem solving ability is affected by many factors, including physiology, personality, and cognition. However, how age and experience influence problem-solving ability during development is harder to untangle. We tested how age and experience affected problem solving in a native Australian rodent, the fawn-footed mosaic-tailed rat Melomys cervinipes. Juveniles were divided into two groups (different ages at start of testing) and then received a food-baited cardboard matchbox every 10days for a total of three tests. We compared the problem-solving ability of individuals from both groups, which allowed us to separate the effects of age and experience. Juveniles with more experience solved the task faster than juveniles with less experience. Furthermore, inexperienced older juveniles interacted with the problems more than inexperienced younger juveniles. Previous solving experience may be important for short-term solving success, while age, in the absence of experience, might be associated with increased exploration, leading to increased investigation of novel problems. Previous experience at manipulating objects generally may also be important for problem-solving success, which likely provides an advantage as resources and habitats change seasonally and annually.

Problem solving in fawn-footed mosaic-tailed rats Melomys cervinipes is not significantly influenced by maternal care or genetic effects.

Innovative problem solving is thought to be a flexible trait that allows animals to adjust to changing or challenging environmental conditions. However, it is not known how problem solving develops during an animal's early life, or whether it may have a heritable component. We investigated whether maternal genetic and nongenetic effects influenced problem-solving ability in a native Australian rodent, the fawn-footed mosaic-tailed rat Melomys cervinipes. We measured direct (time spent grooming and huddling), indirect (time spent nesting), and total amount of maternal care received across pup development (postnatal Days 1-13). We measured problem solving in juveniles using matchbox tasks, and in mothers and adult offspring using six tasks of varying complexity (matchbox, cylinder, obstruction, pillar, tile, and lever tasks). We found no relationship between any maternal care measures and problem-solving abilities across multiple tests, suggesting limited (if any) maternal nongenetic effects. We also found that, as shown by low heritability estimates, problem solving only had a small heritable component in some tasks, but this was nonsignificant and requires further investigation. These results suggest that problem solving is unlikely to be constrained by maternal effects experienced during early development, and is, instead, more likely to be influenced by other factors (e.g., experience) later in an individual's lifetime.

Understanding dispersal patterns can inform future translocation strategies: A case study of the threatened greater stick‐nest rat (Leporillus conditor)

AbstractDispersal behaviour and sociality are significant factors influencing survival at both the individual and population levels. In translocation and breeding programmes, social structure and sex‐biased philopatry and dispersal should be considered in order to maximise population viability and conservation outcomes. Here, we use the greater stick‐nest rat (Leporillus conditor), a native Australian rodent, as a case study to understand how knowledge of social structure and dispersal can inform conservation and translocation programmes. We combine high‐throughput DNA sequencing with field trapping data from a translocated population of greater stick‐nest rats at Arid Recovery Reserve, South Australia, to provide the first empirical evidence of female philopatry and male‐biased dispersal in this species. Males were found to disperse, on average, 1.5 km from the natal nest, while females typically did not disperse beyond 500 m. Further, recapture data showed that females demonstrated a higher degree of nest fidelity than males over time. Based on these findings, we make two key recommendations for future translocations of the species. Firstly, founders should be harvested in small groups at adjacent nest sites with groups separated by a minimum of 1.5 km allowing family group structure to be retained during translocation while simultaneously maximising genetic diversity. Secondly, translocated individuals should be released in family cohorts into patches of optimal habitat that contain adequate shelter substrates interspersed over short distances (~300–500 m, the maximum dispersal distance of females found in this study), thereby facilitating nest establishment and maintenance of family groups. The results of this study have implications for conservation and reintroduction biology as a whole; we highlight the importance of considering spatial genetic structure during all stages of translocations to improve outcomes, and the value of combining genetic and field data to better understand species’ social and spatial preferences.

Exploration influences problem solving in the fawn‐footed mosaic‐tailed rat (Melomys cervinipes)

AbstractThe relationship between an animal's personality and its problem solving ability has become a popular topic of investigation. However, results are conflicting, suggesting that these relationships may be species‐specific. We investigated these relationships in a native Australian rodent, the fawn‐footed mosaic‐tailed rat (Melomys cervinipes). We predicted that more exploratory and less anxious mosaic‐tailed rats would be better problem solvers (e.g. faster to solve the problem) as they would interact with the puzzles more and would be more willing to engage with the task. We assessed personality across two contexts (exploration in an open field and novel object test, and anxiety under simulated predation risk in a light/dark box) and over time (three repetitions). We measured problem solving using two food‐baited puzzle boxes (matchbox and cylinder), a Trixie Dog Activity Board with three problems (pillars, tiles and levers) and an obstruction task. Individual mosaic‐tailed rats showed consistent individual differences in personality, but not problem solving ability. Furthermore, we found a positive relationship between personality and problem solving ability, with more exploratory individuals solving more problems, and solving problems faster, than less exploratory individuals. Exploratory individuals could be better problem solvers because they are more willing to interact with objects and are less neophobic than less exploratory individuals. However, less exploratory individuals still persist in the population, possibly due to differences in cognitive abilities, such as discrimination or recognition, that allow them to compensate for poorer problem solving abilities.

Growth and behavioural development of the fawn-footed mosaic-tailed rat (Melomys cervinipes)

The fawn-footed mosaic-tailed rat (Melomys cervinipes) is a common Australian rainforest rodent; however, little is known about the growth or behavioural development of individuals of this species. We raised mosaic-tailed rats in captivity to assess the growth and behavioural development of pups from birth until weaning. Pups developed quickly compared with some other Australian species, and there were no significant differences in growth between males and females, except for anogenital distance. The auditory meatus was open by Postnatal Day 5, and eyes were fully opened by Postnatal Day 9. All behaviours, including righting, locomotion, negative geotaxis, climbing and grip reflex, were fully developed by Postnatal Day 6. These results suggest that mosaic-tailed rats are semiprecocial in their physical and behavioural development compared with some native Australian rodent species that are found in arid environments. As females produce few, relatively well-developed young, the population has a low intrinsic rate of natural increase. This may, however, be offset by mosaic-tailed rats producing more litters per year. Understanding the biology of mosaic-tailed rats in general could provide insights into how rarer precocial species might struggle to increase in population size under increasing disturbances.

Innovation in a native Australian rodent, the fawn-footed mosaic-tailed rat (Melomys cervinipes).

Innovation is the ability to use a new behaviour, or use an existing behaviour in a new context. Innovation, as an aspect of behavioural flexibility, could be important for allowing animals to cope with rapid environmental changes. Surprisingly, few studies have focused on how innovation ability is affected by task complexity. We investigated innovation ability across multiple tasks of varying complexity in a native Australian rodent, the fawn-footed mosaic-tailed rat (Melomys cervinipes). We predicted that mosaic-tailed rats would be capable of innovating because they live in complex habitats and can exploit disturbed and changing environments. However, we also predicted that the success rate of innovating would decrease as task complexity increased. Mosaic-tailed rats were exposed to six novel problems: cylinder, matchbox, obstruction test, pillar, tile and lever (the last three presented in a Trixie dog activity board), which represented increasing complexity. We counted the number of individuals that could solve at least one task, compared individuals for solving efficiency and latency to solve, and compared the solving success of each task. All mosaic-tailed rats could innovate. However, solving success differed between individuals, with some solving every task and others only solving one. Solving success rate was significantly higher in the simplest task (pillar) compared to the most complicated task (lever). There was no effect of sex or sampling condition on innovation. This study is the first to demonstrate innovation ability across task complexity in an Australian rodent and provides promising avenues for future studies of innovation.

Bias averted: personality may not influence trappability

If bold animals are more likely to be trapped than shy animals, we take a biased sample of personalities—a problem for behavioural research. Such a bias is problematic, also, for population estimation using mark-recapture models that assume homogeneity in detection probabilities. In this study, we investigated whether differences in boldness result in differences in detection probability in a native Australian rodent, the grassland melomys (Melomys burtoni). During a mark-recapture study of this species, we used modified open field tests to assess the boldness (via emergence, and interaction with a novel object) of melomys trapped on the last night of four trapping nights in each of two trapping sessions. Despite melomys showing repeatable variation in these behavioural traits, neither boldness nor emergence latency had an effect on detection probability, and we found no evidence that detection probability varied between individuals. This result suggests that any neophobia is experienced and resolved in individuals of this species on a scale of minutes, rather than the hours across which traps are made available each night. Our work demonstrates that personality-caused sampling bias may not be inevitable, even in situations where animals are required to respond to novelty to be detected, such as in baited traps. Heterogeneity in personality does not inevitably lead to heterogeneity in detection probability. Historically, passive traps were assumed a non-biased means of sampling animal populations. Increasingly behavioural ecologists suggest that personality traits, particularly individual boldness, may influence behaviour and, as a consequence, could result in sampling bias. Here, we present a comprehensive example of when animal personality has no effect on detection probability. Despite having distinct personalities, detection probabilities of a native Australian rodent, grassland melomys Melomys burtoni, were not influenced by whether they were ‘shy’ or ‘bold’. We provide evidence that heterogeneity in personality does not inevitably lead to heterogeneity in detection probability. Given that population estimation models typically assume homogeneity in detection probability between individuals, if this is a broad phenomenon, consistently similar results may improve our confidence in this assumption.

Olfactory recognition of snake cues by fawn-footed mosaic-tailed rats Melomys cervinipes

Abstract Rodents rely on their sensitive olfactory systems to detect and respond to predators. We investigated the ability of a native Australian rodent, the fawn-footed mosaic-tailed rat Melomys cervinipes, to detect, recognise, and discriminate between two species of native snakes. We used snake sheds from a sympatric venomous red-bellied black snake Pseudechis porphyriacus and a non-sympatric non-venomous Stimson’s python Antaresia stimsoni. 20 mosaic-tailed rats each experienced three olfactory tests using a Y-maze. Rats were first exposed to one snake shed against a paper control, and then exposed to the other snake shed against a paper control. Which rat experienced which shed first was allocated randomly. Mosaic-tailed rats were then exposed to both sheds simultaneously. Rats could detect the snake sheds, spending longer investigating, and making more visits to, the sheds than the paper control. They also recognised the sheds as potentially dangerous, reducing their total investigation over time, but increasing their frequency of visits. However, rats did not discriminate between sheds, suggesting a general strategy for assessing the identity of reptilian predators.

Fire affects microhabitat selection, movement patterns, and body condition of an Australian rodent ( Rattus fuscipes )

Abstract Resource selection by animals influences individual fitness, the abundance of local populations, and the distribution of species. Further, the degree to which individuals select particular resources can be altered by numerous factors including competition, predation, and both natural- and human-induced environmental change. Understanding the influence of such factors on the way animals use resources can guide species conservation and management in changing environments. In this study, we investigated the effects of a prescribed fire on small-scale (microhabitat) resource selection, abundance, body condition, and movement pathways of a native Australian rodent, the bush rat ( Rattus fuscipes ). Using a before-after, control-impact design, we gathered data from 60 individuals fitted with spool and line tracking devices. In unburnt forest, selection of resources by bush rats was positively related to rushes, logs and complex habitat, and negatively related to ferns and litter. Fire caused selection for spreading grass, rushes, and complex habitat to increase relative to an unburnt control location. At the burnt location after the fire, rats selected patches of unburnt vegetation, and no rats were caught at a trapping site where most of the understory had been burnt. The fire also reduced bush rat abundance and body condition and caused movement pathways to become more convoluted. After the fire, some individuals moved through burnt areas but the majority of movements occurred within unburnt patches. The effects of fire on bush rat resource selection, movement, body condition, and abundance were likely driven by several linked factors including limited access to shelter and food due to the loss of understory vegetation and heightened levels of perceived predation risk. Our findings suggest the influence of prescribed fire on small mammals will depend on the resulting mosaic of burnt and unburnt patches and how well this corresponds to the resource requirements of particular species.

Discovery of a novel retrovirus sequence in an Australian native rodent (Melomys burtoni): a putative link between gibbon ape leukemia virus and koala retrovirus.

Gibbon ape leukaemia virus (GALV) and koala retrovirus (KoRV) share a remarkably close sequence identity despite the fact that they occur in distantly related mammals on different continents. It has previously been suggested that infection of their respective hosts may have occurred as a result of a species jump from another, as yet unidentified vertebrate host. To investigate possible sources of these retroviruses in the Australian context, DNA samples were obtained from 42 vertebrate species and screened using PCR in order to detect proviral sequences closely related to KoRV and GALV. Four proviral partial sequences totalling 2880 bases which share a strong similarity with KoRV and GALV were detected in DNA from a native Australian rodent, the grassland melomys, Melomys burtoni. We have designated this novel gammaretrovirus Melomys burtoni retrovirus (MbRV). The concatenated nucleotide sequence of MbRV shares 93% identity with the corresponding sequence from GALV-SEATO and 83% identity with KoRV. The geographic ranges of the grassland melomys and of the koala partially overlap. Thus a species jump by MbRV from melomys to koalas is conceivable. However the genus Melomys does not occur in mainland South East Asia and so it appears most likely that another as yet unidentified host was the source of GALV.

Predation on invasive cane toads (Rhinella marina) by native Australian rodents

The success of an invasive species can be reduced by biotic resistance from the native fauna. For example, an invader that is eaten by native predators is less likely to thrive than one that is invulnerable. The ability of invasive cane toads (Rhinella marina) to spread through Australia has been attributed to the toad’s potent defensive chemicals that can be fatal if ingested by native snakes, lizards, marsupials and crocodiles. However, several taxa of native insects and birds are resistant to cane toad toxins. If native rodents are also capable of eating toads (as suggested by anecdotal reports), these large, abundant and voracious predators might reduce toad numbers. Our field observations and laboratory trials confirm that native rodents (Melomys burtoni, Rattus colletti and Rattus tunneyi) readily kill and consume cane toads (especially small toads), and are not overtly affected by toad toxins. Captive rodents did not decrease their consumption of toads over successive trials, and ate toads even when alternative food types were available. In combination with anecdotal reports, our data suggest that rodents (both native and invasive) are predators of cane toads in Australia. Despite concerns about the decline of rodents following the invasion of toads, our data suggest that the species we studied are not threatened by toads as toxic prey, and no specific conservation actions are required to ensure their persistence.

Risky Business: Do Native Rodents Use Habitat and Odor Cues to Manage Predation Risk in Australian Deserts?

In open, arid environments with limited shelter there may be strong selection on small prey species to develop behaviors that facilitate predator avoidance. Here, we predicted that rodents should avoid predator odor and open habitats to reduce their probability of encounter with potential predators, and tested our predictions using a native Australian desert rodent, the spinifex hopping-mouse (Notomys alexis). We tested the foraging and movement responses of N. alexis to non-native predator (fox and cat) odor, in sheltered and open macro- and microhabitats. Rodents did not respond to predator odor, perhaps reflecting the inconsistent selection pressure that is imposed on prey species in the desert environment due to the transience of predator-presence. However, they foraged primarily in the open and moved preferentially across open sand. The results suggest that N. alexis relies on escape rather than avoidance behavior when managing predation risk, with its bipedal movement probably allowing it to exploit open environments most effectively.

The Epidemiology of Koala Retrovirus

A novel Gammaretrovirus, named Koala retrovirus (KoRV) was identified in koalas in 2000. Subsequent testing has shown that KoRV appears to be widespread throughout the wild koala population in Australia. KoRV is apparently unique in that it is the only known example of an exogenous retrovirus which is actively undergoing the process of endogenisation. While there is currently little direct evidence that KoRV causes overt disease in koalas, it is possible or even likely that KoRV infection plays a significant role in the pathogenesis of various neoplasms and a variety of immunosuppressive disorders which are commonly diagnosed in koalas. It appears that KoRV may have arisen through the cross species transmission of a closely related retrovirus in a native Australian rodent, the grassland melomys. Both of these viruses are closely related to a third retrovirus, Gibbon ape leukaemia virus (GALV). GALV was first isolated in the late 1960's from captive gibbons in Thailand that were suffering from leukaemia. To date, the source of GALV remains unknown.

The impact of fossil calibrations, codon positions and relaxed clocks on the divergence time estimates of the native Australian rodents (Conilurini)

The native rodents are the most species-rich placental mammal group on the Australian continent. Fossils of native Australian rodents belonging to the group Conilurini are known from Northern Australia at 4.5Ma. These fossil assemblages already display a rich diversity of rodents, but the exact timing of their arrival on the Australian continent is not yet established. The complete mitochondrial genomes of two native Australian rodents, Leggadina lakedownensis (Lakeland Downs mouse) and Pseudomys chapmani (Western Pebble-mound mouse) were sequenced for investigating their evolutionary history. The molecular data were used for studying the phylogenetic position and divergence times of the Australian rodents, using 12 calibration points and various methods.Phylogenetic analyses place the native Australian rodents as the sister-group to the genus Mus. The Mus–Conilurini calibration point (7.3–11.0Ma) is highly critical for estimating rodent divergence times, while the influence of the different algorithms on estimating divergence times is negligible. The influence of the data type was investigated, indicating that amino acid data are more likely to reflect the correct divergence times than nucleotide sequences.The study on the problems related to estimating divergence times in fast-evolving lineages such as rodents, emphasize the choice of data and calibration points as being critical. Furthermore, it is essential to include accurate calibration points for fast-evolving groups, because the divergence times can otherwise be estimated to be significantly older. The divergence times of the Australian rodents are highly congruent and are estimated to 6.5–7.2Ma, a date that is compatible with their fossil record.

Breeding and maintenance of the Central rock‐rat Zyzomys pedunculatus at Perth Zoo

The Central rock‐rat Zyzomys pedunculatus is a native Australian rodent, thought to be extinct until its rediscovery near Alice Springs in 1996. Classified as Critically Endangered, recovery actions include the study and maintenance of the species in captivity. Between mid‐2001 and mid‐2002, eight litters were produced at Perth Zoo, with 26 young surviving to weaning. Females were shown to be capable of producing three to four young every 37–44 days. The husbandry protocols, reproductive parameters, reproductive behaviour, and birth and development of young Z. pedunculatus are described in this article.

The distribution of renal hyaluronan and the expression of hyaluronan synthases during water deprivation in the Spinifex hopping mouse, Notomys alexis

Hyaluronan (HA) is a glycosaminoglycan that is synthesized by a family of enzymes called hyaluronan synthases (HASs), of which there are three isoforms (HAS1, 2 and 3) in mammals. The HASs have different tissue expression patterns and function, indicating that synthesis of HA and formation of the HA matrix may be regulated by various factors. The HA matrix has an important role in renal water handling and the production of a concentrated urine. We investigated the distribution of HA and the expression of HAS1, HAS2 and HAS3 mRNAs in the kidney of the Spinifex hopping mouse, Notomys alexis, a native Australian desert rodent that is reported to produce the most concentrated urine of any mammal. After periods of three, seven and fourteen days of water deprivation, the distribution of renal HA changed considerably, and there was a general down-regulation of HAS mRNA expression. It is proposed that the regulation of HA synthesis by the different HAS isoforms during water deprivation in N. alexis, could be influenced by the molecular mass of the HA chains produced by each isoform, followed by the rate at which the individual HAS produces HA.