In situ predator conditioning of naive prey prior to reintroduction.

Many translocations and introductions to recover threatened populations fail because predators kill prey soon after release; a problem exacerbated for predator-naive prey. While pre-release training has been shown to work in some situations, it is time consuming and relies on using inferred predator cues and treating small groups. We review a relatively new and very promising management tool: in situ, pre-release predator conditioning. Here, the goal is to allow prey in large enclosures to live with low densities of predators to accelerate selection for antipredator traits (in an evolutionary sense) or provide prey essential experience with predators that they will later encounter. We review the published results of a large-scale, controlled experiment where we have permitted burrowing bettongs (Bettongia lesueur) and greater bilblies (Macrotis lagotis) to live with low densities of feral cats (Felis catus), a species implicated in their widespread decline and localized extinction. We found that both species could persist with cats, suggesting that future work should define coexistence thresholds-which will require knowledge of prey behaviour as well as the structure of the ecological community. Compared to control populations, predator-naive prey exposed to cats has a suite of morphological and behavioural responses that seemingly have increased their antipredator abilities. Results suggest that predator-conditioned bilbies survive better when released into a large enclosure with an established cat population; future work will determine whether this increased survival extends to the wild. This article is part of the theme issue 'Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation'.

Cancer- and behavior-related genes are targeted by selection in the Tasmanian devil (Sarcophilus harrisii).

Devil Facial Tumor Disease (DFTD) is an aggressive cancer notorious for its rare etiology and its impact on Tasmanian devil populations. Two regions underlying an evolutionary response to this cancer were recently identified using genomic time-series pre- and post-DTFD arrival. Here, we support that DFTD shaped the genome of the Tasmanian devil in an even more extensive way than previously reported. We detected 97 signatures of selection, including 148 protein coding genes having a human orthologue, linked to DFTD. Most candidate genes are associated with cancer progression, and an important subset of candidate genes has additional influence on social behavior. This confirms the influence of cancer on the ecology and evolution of the Tasmanian devil. Our work also demonstrates the possibility to detect highly polygenic footprints of short-term selection in very small populations.

The role of basking in the development of endothermy and torpor in a marsupial.

Marsupials have a slow rate of development and this allows a detailed examination of thermoregulatory developmental changes and stages. We quantified the cooling rates of marsupial dunnarts (Sminthopsis crassicaudata) at 40-56 days (d) old, and torpor and basking behaviour in animals given the option to bask in four age groups from 60 to 150 d. The development of thermoregulation was a continuum, but was characterised by three major thermoregulatory stages: (1) at 40 d, animals were unable to maintain a constant high body temperature during short-term cold exposure; (2) at 60 d, animals could maintain a high T b for the first part of the night at an ambient temperature of 15.0 ± 0.7 °C; later in the night, they entered an apparent torpor bout but could only rewarm passively when basking under a heat lamp; (3) from ~90 d, they expressed prolonged torpor bouts and were able to rewarm endogenously. Young newly weaned 60 d animals were able to avoid hypothermia by basking. In this case, basking was not an optional behavioural method of reducing the cost of rewarming from torpor, but was essential for thermoregulation independent of the nest temperature. Results from our study suggest that basking is a crucial behavioural trait that permits young marsupials and perhaps other juvenile altricial mammals to overcome the developmental stage between poikilothermy early in development and full endothermy later in life.

Phenotypic plasticity of post-fire activity and thermal biology of a free-ranging small mammal.

Ecosystems can change rapidly and sometimes irreversibly due to a number of anthropogenic and natural factors, such as deforestation and fire. How individual animals exposed to such changes respond behaviourally and physiologically is poorly understood. We quantified the phenotypic plasticity of activity patterns and torpor use - a highly efficient energy conservation mechanism - in brown antechinus (Antechinus stuartii), a small Australian marsupial mammal. We compared groups in densely vegetated forest areas (pre-fire and control) with a group in a burned, open habitat (post-fire). Activity and torpor patterns differed among groups and sexes. Females in the post-fire group spent significantly less time active than the other groups, both during the day and night. However, in males only daytime activity declined in the post-fire group, although overall activity was also reduced on cold days in males for all groups. The reduction in total or diurnal activity in the post-fire group was made energetically possible by a ~3.4-fold and ~2.2-fold increase in the proportion of time females and males, respectively, used torpor in comparison to that in the pre-fire and control groups. Overall, likely due to reproductive needs, torpor was more pronounced in females than in males, but low ambient temperatures increased torpor bout duration in both sexes. Importantly, for both male and female antechinus and likely other small mammals, predator avoidance and energy conservation - achieved by reduced activity and increased torpor use - appear to be vital for post-fire survival where ground cover and refuges have been obliterated.

Friends with benefits: the role of huddling in mixed groups of torpid and normothermic animals.

Huddling and torpor are widely used for minimizing heat loss by mammals. Despite the questionable energetic benefits from social heterothermy of mixed groups of warm normothermic and cold torpid individuals, the heterothermic Australian sugar glider (Petaurus breviceps) rests in such groups during the cold season. To unravel why they might do so, we examined torpor expression of two sugar glider groups of four individuals each in outside enclosures during winter. We observed 79 torpor bouts during 50 days of observation and found that torpor bouts were longer and deeper when all individuals of a group entered torpor together, and therefore infer that they would have saved more energy in comparison to short and shallow solitary torpor bouts. However, all gliders of either group only expressed torpor uniformly in response to food restriction, whereas on most occasions at least one individual per group remained normothermic. Nevertheless, the presence of warm gliders in mixed groups also appears to be of energetic advantage for torpid individuals, because nest box temperature was negatively correlated with the number of torpid gliders, and normothermic individuals kept the nest temperature at a value closer to the threshold for thermoregulatory heat production during torpor. Our study suggests that mixed groups of torpid and normothermic individuals are observed when environmental conditions are adverse but food is available, leading to intermediate energy savings from torpor. However, under especially challenging conditions and when animals are starving, energy savings are maximized by uniform and pronounced expression of torpor.

Physiological and behavioural responses of a small heterothermic mammal to fire stimuli.

The predicted increase of the frequency and intensity of wildfires as a result of climate change could have a devastating impact on many species and ecosystems. However, the particular physiological and behavioural adaptions of animals to survive fires are poorly understood. We aimed to provide the first quantitative data on physiological and behavioural mechanisms used by a small heterothermic marsupial mammal, the fat-tailed dunnart (Sminthopsis crassicaudata), that may be crucial for survival during and immediately after a fire. Specifically, we aimed to determine (i) whether captive torpid animals are able to respond to fire stimuli and (ii) which energy saving mechanisms are used in response to fires. The initial response of torpid dunnarts to smoke exposure was to arouse immediately and therefore express shorter and shallower torpor bouts. Dunnarts also increased activity after smoke exposure when food was provided, but not when food was withheld. A charcoal/ash substrate, imitating post-fire conditions, resulted in a decrease in torpor use and activity, but only when food was available. Our novel data suggests that heterothermic mammals are able to respond to fire stimuli, such as smoke, to arouse from torpor as an initial response to fire and adjust torpor use and activity levels according to food availability modulated by fire cues.

Huddling behaviour and energetics of Sminthopsis spp. (Marsupialia, Dasyruidae) in response to environmental challenge.

We describe how behavioural responses are an important adjunct to physiological responses for two dunnart marsupials that live in arid environments. Behavioural responses of the stripe-faced dunnart Sminthopsis macroura and the Ooldea dunnart Sminthopsis ooldea differed with acclimation to four ambient temperature (T(a)) regimes, 12 h:12 h of 5-15 °C, 12-22 °C, 18-28 °C and 25-35 °C. Aggression levels were low at regimes 5-15 °C and 12-22 °C, and high at regimes 18-28 °C and 25-35 °C. The proportion of S. macroura huddled in groups increased significantly with decreasing T(a) regime, but there was no aggregation by S. ooldea at low T(a) regimes. The energetic benefit of huddling by S. macroura was highest for pairs of dunnarts (27% saving compared with singles) and only 3% for triplets at T(a)=10 °C. Thermal conductance decreased for pairs but not triplets compared to singles. There were no energetic savings for S. ooldea with increased numbers, and thermal conductance was the same per individual for single, pairs and triplets, reflecting their lack of huddling behaviour. The flexible behavioural (huddling) responses of S. macroura may facilitate their capacity to occupy a broad geographical distribution, unlike S. ooldea, which had inflexible behavioural responses (no huddling) and has a more restricted geographical range. The phylogenetic relationships of the dunnarts suggest that social behaviours may have arisen only once in the most adaptable subgroup of the Sminthopsini.

Evaluating and approaching a strange animal: children's trust in informant testimony.

This study examined 3- to 7-year-old children's reliance on informant testimony to learn about a novel animal. Sixty participants were given positive or negative information about an Australian marsupial from an informant described as a maternal figure or a zookeeper. Children were asked which informant was correct and were invited to touch the animal, which was a stuffed toy hidden in a crate. Overall, younger children endorsed the zookeeper's testimony about the animal, but touched the animal more readily when the maternal figure provided positive information. Older children endorsed the informant who provided positive information, but showed some sensitivity to zookeeper expertise. Age differences were obtained in the association between participant characteristics and informant selection and animal approach behavior.

Lateralisation of escape responses in the stripe-faced dunnart, Sminthopsis macroura (Dasyuridae: Marsupialia).

Although lateralisation has been observed in many vertebrate species, marsupials have been neglected in the study of lateralisation. We investigated the behavioural responses of the stripe-faced dunnart (Sminthopsis macroura) to a mechanical model of a snake approaching into the monocular (left and right) or the binocular visual field. The snake model was presented to 30 adult subjects. The behavioural responses and the latency to react to the stimulus were scored. Reactivity was calculated by pooling scores for retreat, startle, ears back, and orientation. Retreat tended to be the most common of these responses. Approach of the snake into the dunnarts' left monocular visual field elicited a significantly higher reactivity compared to approach into the right or binocular visual field. Half of the animals did not respond in the 60 seconds allocated when the stimulus approached on their right side, whereas only seven did not respond when the stimulus approached on the left, and ten when the stimulus was presented binocularly. These results are consistent with the right hemisphere's known specialisation for controlling fear and escape responses. Our results suggest that marsupials are lateralised in a way similar to other vertebrates.

Studies of learning and problem solving in two species of Australian marsupials.

This article reviews the authors' recent work with two species of Australian marsupials on several learning and conditioning experiments. The quokka (Setonix brachyurus) is a cat-sized herbivorous wallaby that inhabits offshore islands around south-western Australia. The fat-tailed dunnart (Sminthopsis crassicaudata) is a mouse-sized carnivorous marsupial that inhabits much of inland Australia. Both species were successful in learning simple discriminations, learning sets and reversal sets. Quokkas and dunnarts were also tested on two configural discrimination tasks: transverse patterning and negative patterning; only the dunnarts successfully solved these tasks. Dunnarts were also the only species to show one-trial learning in reversal set training. Dunnarts may be particularly useful subjects in future studies of brain-behavior relationships, since these animals have some interesting neuroanatomical features, demonstrate a wide range of fast learning abilities, and as pouch young, can be accessed during early developmental stages.

Configural learning in two species of marsupial (Setonix brachyurus and Sminthopsis crassicaudata).

Four experiments examined the ability of quokkas (Setonix brachyurus) and fat-tailed dunnarts (Sminthopsis crassicaudata) to solve 2 configural tasks: transverse and negative patterning. Transverse patterning requires the simultaneous solution of 3 overlapping discrimination problems (A+ B-, B+ C-, C+ A-). Both species could solve the nonoverlapping (elemental) version of this task (U+ V-, W+ X-, Y+ Z-), but only dunnarts solved the transverse patterning task. Negative patterning requires conditioned responses to 2 stimuli when presented separately but not together (A+, B+, AB-). Both species formed a selective conditioned response to A+ and B+ stimuli and inhibited responding to a simple nonreinforced stimulus (C-), but only dunnarts successfully inhibited responding to the AB- compound to solve the negative patterning task. These experiments are the first to demonstrate configural learning in a marsupial.

Visual discrimination learning and strategy behavior in the fat-tailed dunnart (Sminthopsis crassicaudata).

Fat-tailed dunnarts (Sminthopsis crassicaudata) were trained on visual discrimination learning-set, reversal-set, and spatial delayed-alternation tasks. The learning set involved 36 2-way black-and-white pattern discriminations and 5 probe reversals. Ten reversals of a black-and-white pattern discrimination were followed by 5 novel tasks. Spatial alternation was tested at delays up to 20 s. Learning-set and reversal-set formation, including 1-trial learning and spontaneous transfer from learning set to reversals and vice versa, was found. Learning-set-experienced dunnarts showed no retention of previously learned tasks 1 week after testing but demonstrated consistently high Trial 2 performance, indicating the retention of a response strategy. Delayed-alternation tasks were learned up to 10-s delays. These results provide the first evidence of a visually guided "win-stay, lose-shift" strategy in a marsupial.

Do big-brained animals play more? Comparative analyses of play and relative brain size in mammals.

It has been hypothesized that play is more likely to be present in larger brained species. We tested this hypothesis in mammals using independent contrasts, a method that controls for phylogenetic relatedness. Comparisons across 15 orders revealed that the prevalence and complexity of play was significantly correlated with brain size, with larger brained orders having more playful species. Three orders, Rodentia, Marsupialia, and Primates, were used for within-order comparisons among species and, where possible, among families. The comparisons were not significant for rodents or primates, and those for marsupials yielded inconsistent results. Therefore, although a strong relationship is present at the highest taxonomic level of comparison, it diminishes or evaporates at lower level comparisons.

Phylogeographical population structure of tiger quolls Dasyurus maculatus (Dasyuridae: Marsupialia), an endangered carnivorous marsupial.

Tiger quolls, Dasyurus maculatus, are the largest carnivorous marsupials still extant on the mainland of Australia, and occupy an important ecological niche as top predators and scavengers. Two allopatric subspecies are recognized, D.m. gracilis in north Queensland, and D.m. maculatus in the southeast of the mainland and Tasmania. D.m. gracilis is considered endangered while D.m. maculatus is listed as vulnerable to extinction; both subspecies are still in decline. Phylogeographical subdivision was examined to determine evolutionarily significant units (ESUs) and management units (MUs) among populations of tiger quolls to assist in the conservation of these taxa. Ninety-three tiger quolls from nine representative populations were sampled from throughout the species range. Six nuclear microsatellite loci and the mitochondrial DNA (mtDNA) control region (471 bp) were used to examine ESUs and MUs in this species. We demonstrated that Tasmanian tiger quolls are reciprocally monophyletic to those from the mainland using mtDNA analysis, but D.m. gracilis was not monophyletic with respect to mainland D.m. maculatus. Analysis of microsatellite loci also revealed significant differences between the Tasmanian and mainland tiger quolls, and between D.m. gracilis and mainland D.m. maculatus. These results indicate that Tasmanian and mainland tiger quolls form two distinct evolutionary units but that D.m. gracilis and mainland D.m. maculatus are different MUs within the same ESU. The two marker types used in this study revealed different male and female dispersal patterns and indicate that the most appropriate units for short-term management are local populations. A revised classification and management plan are needed for tiger quolls, particularly in relation to conservation of the Tasmanian and Queensland populations.