Are Urban Populations of a Gliding Mammal Vulnerable to Decline?

Small populations are at high risk of extinction, and they are likely to need management intervention. Successful management, however, relies on sufficient long-term demographic data in order to determine whether apparent declines are natural fluctuations or the product of threatening processes. In this study, we monitored a small urban population of squirrel gliders (Petaurus norfolcensis) in Queensland, Australia, over a 16 year period. A reference population in a larger forest patch was also studied in order to investigate whether its demographic trends were similar. Using mark-recapture data to generate estimates of apparent survival and population size, we found evidence of a decline within the small population but not in the reference population over the monitoring period. We suggest that the influence of multiple factors may have led to the decline, but, ultimately, that the genetic condition of the small population may be responsible. Understanding demographic trends is an important context for management interventions of small populations, although causes of decline need to be identified for successful management. The squirrel glider provides a useful case study for small urban populations and particularly for arboreal mammals.

Use of road underpasses by mammals and a monitor lizard in eastern Australia and consideration of the prey-trap hypothesis.

Road networks continue to expand globally with predictable effects on ecological systems. Research into the effectiveness of road underpasses and overpasses for wildlife has been concentrated in North America and Europe. In Australia, most studies of underpasses have been of relatively short duration and without reference sites to give context to the measured rates of use. We studied 5-7 road underpasses at two locations in eastern Australia over 2-3 years, comparing camera trap detections of animals in underpasses with those at nearby forest sites. Three species of large macropod (wallabies and kangaroos) were frequently detected in the underpasses, with some underpasses traversed 1-4 times per week, and in many cases exceeded detections in the forest. The lace monitor (Varanus varius) was detected in all underpasses, often once per week during spring and summer, and infrequently in the forest. At each location, a different small macropod species, including one regionally threatened, showed a higher probability of detection in one underpass compared with several of the forest sites. The vulnerable koala (Phascolarctos cinereus) was detected infrequently in underpasses and in the adjoining forest. The short-beaked echidna (Tachyglossus aculeatus) had a high probability of detection in a single underpass. The "prey-trap hypothesis" postulates that predators will exhibit increased activity at underpasses as a consequence of prey being funneled. We found the red fox (Vulpes vulpes) had high activity in some underpasses. However, its activity coincided less than expected with the activity of the mammals most at risk to it. Our results provide no consistent support for the "prey-trap hypothesis." Instead, our study confirms the generic value of underpasses for a range of medium-large mammals as well as one large reptile. Habitat adjoining underpasses exert a strong influence on their use and require greater consideration to maximize underpass use.

Multiyear monitoring of threatened iconic arboreal mammals in a mid-elevation conservation reserve in eastern Australia.

Multiyear investigations of population dynamics are fundamental to threatened species conservation. We used multiseason occupancy based on spotlight surveys to investigate dynamic occupancy of the koala and the greater glider over an 8-year period that encompassed a severe drought in year 6. We combined our occupancy estimates with literature estimates of density to estimate the population sizes of these species within the focal conservation reserve. Both species showed substantial yearly variation in the probability of detection (koala: 0.13-0.24; greater glider: 0.12-0.36). Detection of the koala did not follow any obvious pattern. Low detection of the greater glider coincided with the drought and two subsequent years. We suggest the low detection reflected a decline in abundance. The probability of occupancy of the koala was estimated to be 0.88 (95% CI: 0.75-1.0) in year 8. Autonomous recording units were also used in year 8, enabling an independent occupancy estimate of 0.80 (0.64-0.90). We found no evidence of a drought-induced decline in the koala. Habitat variables had a weak influence on koala occupancy probabilities. The probability of occupancy of the greater glider changed little over time, from 0.52 (95% CI: 0.24-0.81) to 0.63 (0.42-0.85) in year 8. Modeling suggested that the probability of colonization was positively influenced by the percentage cover of rainforest. Increased cover of these nonbrowse trees may reflect thermal buffering, site productivity, or soil moisture. We estimate that our study reserve is likely to contain >900 adult koalas and >2400 adult greater gliders. These are among some of the first reserve-wide estimates for these species. Our study reserve can play an important role in the conservation of both species.

Tolerance to high temperature by arboreal mammals using nest boxes in southern Australia.

Nest boxes are used to manage populations of tree-cavity dependent birds and mammals. Concerns have been raised that due to their poor insulative properties nest boxes may cause heat stress and occasionally death during summers of extreme maximum temperatures. Our study investigated whether this nest box heat stress hypothesis applies to two small cavity-dependent mammals (brush-tailed phascogales and sugar gliders). Focusing on days when ambient temperature reached ≥40 °C, we recorded: i) temperatures within occupied nest boxes, ii) temperatures within nearby unoccupied tree cavities, iii) the duration of temperatures of ≥40 °C within nest boxes, iv) whether direct mortality was observed, and v) the relative abundance of these species in nest boxes before and after a very hot summer. When ambient temperature reached ≥40 °C, nest boxes were equivalent to ambient or 1-2 °C cooler, whereas tree cavities were 3-7 °C cooler than ambient. Exposure in nest boxes to temperatures of ≥40 °C lasted an average of 2-8 h. We observed no mortality over 65 records of phascogales and 31 records of gliders in nest boxes on days when ambient reached ≥40 °C. No decline in abundance was recorded after a summer with 11 days of temperatures ≥40 °C, with each species subsequently occupying >40 nest boxes. Our observations suggest these species are tolerant of the high temperatures that occurred. Nonetheless, provision of nest boxes designed to minimise summer heating is recommended.

Habitat and introduced predators influence the occupancy of small threatened macropods in subtropical Australia.

Australia has had the highest rate of mammal extinctions in the past two centuries when compared to other continents. Frequently cited threats include habitat loss and fragmentation, changed fire regimes and the impact of introduced predators, namely the red fox (Vulpes vulpes) and the feral cat (Felis catus). Recent studies suggest that Australia's top predator, the dingo (Canis dingo), may have a suppressive effect on fox populations but not on cat populations. The landscape of fear hypothesis proposes that habitat used by prey species comprises high to low risk patches for foraging as determined by the presence and ubiquity of predators within the ecosystem. This results in a landscape of risky versus safe areas for prey species. We investigated the influence of habitat and its interaction with predatory mammals on the occupancy of medium-sized mammals with a focus on threatened macropodid marsupials (the long-nosed potoroo [Potorous tridactylous] and red-legged pademelon [Thylogale stigmatica]). We assumed that differential use of habitats would reflect trade-offs between food and safety. We predicted that medium-sized mammals would prefer habitats for foraging that reduce the risk of predation but that predators would have a positive relationship with medium-sized mammals. We variously used data from 298 camera trap sites across nine conservation reserves in subtropical Australia. Both dingoes and feral cats were broadly distributed, whilst the red fox was rare. Long-nosed potoroos had a strong positive association with dense ground cover, consistent with using habitat complexity to escape predation. Red-legged pademelons showed a preference for open ground cover, consistent with a reliance on rapid bounding to escape predation. Dingoes preferred areas of open ground cover whereas feral cats showed no specific habitat preference. Dingoes were positively associated with long-nosed potoroos whilst feral cats were positively associated with red-legged pademelons. Our study highlights the importance of habitat structure to these threatened mammals and also the need for more detailed study of their interactions with their predators.

Fine-scale genetic response to landscape change in a gliding mammal.

Understanding how populations respond to habitat loss is central to conserving biodiversity. Population genetic approaches enable the identification of the symptoms of population disruption in advance of population collapse. However, the spatio-temporal scales at which population disruption occurs are still too poorly known to effectively conserve biodiversity in the face of human-induced landscape change. We employed microsatellite analysis to examine genetic structure and diversity over small spatial (mostly 1-50 km) and temporal scales (20-50 years) in the squirrel glider (Petaurus norfolcensis), a gliding mammal that is commonly subjected to a loss of habitat connectivity. We identified genetically differentiated local populations over distances as little as 3 km and within 30 years of landscape change. Genetically isolated local populations experienced the loss of genetic diversity, and significantly increased mean relatedness, which suggests increased inbreeding. Where tree cover remained, genetic differentiation was less evident. This pattern was repeated in two landscapes located 750 km apart. These results lend support to other recent studies that suggest the loss of habitat connectivity can produce fine-scale population genetic change in a range of taxa. This gives rise to the prediction that many other vertebrates will experience similar genetic changes. Our results suggest the future collapse of local populations of this gliding mammal is likely unless habitat connectivity is maintained or restored. Landscape management must occur on a fine-scale to avert the erosion of biodiversity.

Degree of landscape fragmentation influences genetic isolation among populations of a gliding mammal.

Forests and woodlands are under continuing pressure from urban and agricultural development. Tree-dependent mammals that rarely venture to the ground are likely to be highly sensitive to forest fragmentation. The Australian squirrel glider (Petaurus norfolcensis) provides an excellent case study to examine genetic (functional) connectivity among populations. It has an extensive range that occurs in a wide band along the east coast. However, its forest and woodland habitat has become greatly reduced in area and is severely fragmented within the southern inland part of the species' range, where it is recognised as threatened. Within central and northern coastal regions, habitat is much more intact and we thus hypothesise that genetic connectivity will be greater in this region than in the south. To test this we employed microsatellite analysis in a molecular population biology approach. Most sampling locations in the highly modified south showed signatures of genetic isolation. In contrast, a high level of genetic connectivity was inferred among most sampled populations in the more intact habitat of the coastal region, with samples collected 1400 km apart having similar genetic cluster membership. Nonetheless, some coastal populations associated with urbanisation and agriculture are genetically isolated, suggesting the historic pattern observed in the south is emerging on the coast. Our study demonstrates that massive landscape changes following European settlement have had substantial impacts on levels of connectivity among squirrel glider populations, as predicted on the basis of the species' ecology. This suggests that landscape planning and management in the south should be focused on restoring habitat connectivity where feasible, while along the coast, existing habitat connectivity must be maintained and recent losses restored. Molecular population biology approaches provide a ready means for identifying fragmentation effects on a species at multiple scales. Such studies are required to examine the generality of our findings for other tree-dependent species.

Experimental Rock Outcrops Reveal Continuing Habitat Disturbance for an Endangered Australian Snake.

Protected areas are commonly viewed as safe havens for endangered species. To test this notion, we experimentally constructed small rock outcrops for the endangered broad-headed snake ( Hoplocephalus bungaroides) within a national park near Sydney, Australia. Rock outcrops provide vital shelter sites during the cooler months of the year. Constructed rock outcrops (3 × 5 m) were placed at 11 paired sites located near (≤250 m) and far from (>400 m) walking tracks and roads. Eight of our 22 rock outcrops were disturbed by people over a 15-month period. Disturbance consisted of displacement of some rocks or complete destruction of the outcrop. Disturbed outcrops occurred up to 450 m from a walking track or road. Disturbance to natural outcrops has also been observed in this park. This demonstrates a continuing decline in the quality of this snake's habitat. Twenty of our rock outcrops were colonized by velvet geckos (Oedura lesueurii), the primary prey of this snake. One broad-headed snake was found in one outcrop. According to these findings, attempts to restore the habitat of this endangered snake should be centered on sites located ≥500 m from a walking track or road. Our study highlights the value of targeted experiments that precede larger-scale habitat restoration.

RESUMEN: Las áreas protegidas son comúnmente vistas como paraísos libres de riesgos para las especies amenazadas. Para probar esta noción, construimos experimentalmente pequeños farallones rocosos para la serpiente amenazada de cabeza ancha ( Hoplocephalus bungaroides) dentro de un parque nacional cercano a Sydney, Australia. Los farallones de roca proveen protección vital durante los meses más fríos del año. Los farallones construidos (3 × 5 m) fueron colocados en once sitios pareados localizados cerca (≤250 m) y lejos (>400 m) de los senderos y carreteras. Ocho de los 22 farallones fueron perturbados por gentes sobre un período de 15 meses. La perturbación consistió en el desplazamiento de algunas rocas o en la completa destrucción del farallón. Los farallones perturbados se encontraban hasta 450 m de los senderos o las carreteras. La perturbación de farallones naturales también ha sido observada en este parque. Esto demuestra una disminución continua de la cantidad de este tipo de hábitat para las serpientes. Veinte de nuestros farallones fueron colonizados por gecos velvet (Oedura lasueurii), la principal presa de esta serpiente. Con base en estos resultados, los intentos para restaurar el hábitat de esta especie de serpiente amenazada deberán centrarse en sitios localizados ≥500 m de los senderos o las carreteras. Nuestro estudio subraya el valor de los experimentos que preceden a esfuerzos de restauración del hábitat a gran escala.

The foraging behaviour of a nectar feeding marsupial, Petaurus australis.

The foraging behaviour of non-flying nectar feeding mammals has been examined rarely. The exudivorous yellow-bellied glider (Petaurus australis) was observed to feed extensively (70% of the total feeding observation time) on the nectar of all species of Eucalyptus present at a site in southeastern Australia. Gliders harvested nectar, and presumably pollen also, whenever eucalypt flowers were available and selected trees with 2-3 times as many flowers as that on trees randomly selected along a transect. The abundance of flowering trees varied temporally and, at times when few flowering trees were present, gliders chose trees with fewer flowers than at times when flowering trees were abundant. When flowering trees were superabundant or scarce, there was no relationship between the number of flowers in a tree and the duration of visits by gliders. However, at intermediate levels of abundance, the amount of time a glider spent in a tree was related to the number of flowers in a tree. Gliders devoted 90% of the time outside their dens to foraging and the above relationship is suggested to reflect two foraging options which maximize net energy gain for different abundances of flowering trees. Although gliders spent considerable lengths of time in individual trees feeding, initial deposition of cross pollen when gliders first arrive in a tree may be substantial and thus, may provide significant amounts of outcrossing for these eucalypts.