Investigation into the utility of flying foxes as bioindicators for environmental metal pollution reveals evidence of diminished lead but significant cadmium exposure

Due to their large range across diverse habitats, flying-foxes are potential bioindicator species for environmental metal exposure. To test this hypothesis, blood spots, urine, fur, liver and kidney samples were collected from grey-headed flying-foxes (Pteropus poliocephalus) and black flying-foxes (P. alecto) from the Sydney basin, Australia. Concentrations of arsenic, cadmium, copper, lead, mercury and zinc and 11 other trace metals were determined using inductively coupled plasma mass spectrometry. As predicted, kidney and fur lead concentrations were lower compared to concentrations found in flying-foxes in the early 1990’s, due to reduced environmental lead emissions. Tissue cadmium concentrations in flying-foxes were higher compared to previous studies of flying-foxes and other bat species, suggesting that flying-foxes were exposed to unrecognized cadmium sources. Identification of these sources should be a focus of future research. Urine concentrations of arsenic, cadmium, mercury, and lead were proportional to kidney concentrations. Given that urine can be collected from flying-foxes without handling, this demonstrates that many flying-foxes can be assessed for metal exposure with relative ease. The analysis of blood spots was not viable because of variable metal concentrations in the filter paper used. Fur concentrations of metals correlated poorly with tissue concentrations at the low levels of metals found in this study, but fur could still be a useful sample if flying-foxes are exposed to high levels of metals. Lastly, heat inactivation had minimal impact on metal concentrations in kidney and liver samples and should be considered as a tool to protect personnel working with biohazardous samples

Human-modified landscapes provide key foraging areas for a threatened flying mammal : the grey-headed flying-fox

Urban expansion is a major threat to natural ecosystems but also creates novel opportunities that adaptable species can exploit. The grey-headed flying-fox (Pteropus poliocephalus) is a threatened, highly mobile species of bat that is increasingly found in human-dominated landscapes, leading to many management and conservation challenges. Flying-fox urbanisation is thought to be a result of diminishing natural foraging habitat or increasing urban food resources, or both. However, little is known about landscape utilisation of flying-foxes in human-modified areas, and how this may differ in natural areas. Here we examine positional data from 98 satellite-tracked P. poliocephalus for up to 5 years in urban and nonurban environments, in relation to vegetation data and published indices of foraging habitat quality. Our findings indicate that human-modified foraging landscapes sustain a large proportion of the P. poliocephalus population year-round. When individuals roosted in nonurban and minor-urban areas, they relied primarily on wet and dry sclerophyll forest, forested wetlands, and rainforest for foraging, and preferentially visited foraging habitat designated as high-quality. However, our results highlight the importance of human-modified foraging habitats throughout the species’ range, and particularly for individuals that roosted in major-urban environments. The exact plant species that exist in human-modified habitats are largely undocumented; however, where this information was available, foraging by P. poliocephalus was associated with different dominant plant species depending on whether individuals roosted in ‘urban’ or ‘non-urban’ areas. Overall, our results demonstrate clear differences in urban- and non-urban landscape utilisation by foraging P. poliocephalus. However, further research is needed to understand the exact foraging resources used, particularly in human-modified habitats, and hence what attracts flying-foxes to urban areas. Such information could be used to modify the urban foraging landscape, to assist long-term habitat management programs aimed at minimising human-wildlife conflict and maximising resource availability within and outside of urban environments

Evidence of chronic cadmium exposure identified in the critically endangered Christmas Island flying-fox (Pteropus natalis)

The Christmas Island flying-fox (Pteropus natalis) is the last native mammal on Christmas Island and its population is in decline. Phosphate mining occurs across much of the eastern side of Christmas Island. The phosphate deposits are naturally rich in cadmium, and potentially other metals, which may be threatening the Christmas Island flying-fox population. To test this, concentrations of metals (cadmium, copper, iron, mercury, lead, and zinc) were measured in fur and urine collected from Christmas Island flying-foxes and interpreted concurrently with urinalysis and serum biochemistry data. In addition, metal concentrations in liver and kidney samples from two Christmas Island flying-foxes and associated histological findings from one of these individuals are reported. Fur cadmium concentrations were significantly higher in the Christmas Island flying-fox compared to concentrations found in flying-foxes in mainland Australia. Additionally, 30% of Christmas Island flying-foxes had urine cadmium concentrations exceeding maximum concentrations previously reported in flying-foxes in mainland Australia. Glucosuria and proteinuria were identified in two Christmas Island flying-foxes, suggestive of renal dysfunction. In one aged flying-fox, kidney cadmium concentrations were four-fold higher than toxic thresholds reported for domestic mammals. Microscopic evaluation of this individual identified bone lesions consistent with those described in laboratory animals with chronic cadmium poisoning. These results suggest that Christmas Island flying-foxes are being exposed to cadmium and identification of these sources is recommended as a focus of future research. Unexpectedly, urine iron concentrations in Christmas Island flying-foxes were higher compared to previous studies of Australian mainland flying-foxes, which suggests that urinary excretion of iron may be an important aspect of iron homeostasis in this species whose diet is iron rich

Staying in touch : how highly specialised moth pollinators track host plant phenology in unpredictable climates

Background: For specialised pollinators, the synchrony of plant and pollinator life history is critical to the persistence of pollinator populations. This is even more critical in nursery pollination, where pollinators are obligately dependant on female host plant flowers for oviposition sites. Epicephala moths (Gracillariidae) form highly specialised nursery pollination mutualisms with Phyllanthaceae plants. Several hundred Phyllanthaceae are estimated to be exclusively pollinated by highly specific Epicephala moths, making these mutualisms an outstanding example of plant–insect coevolution. However, there have been no studies of how Epicephala moths synchronise their activity with host plant flowering or persist through periods when flowers are absent. Such knowledge is critical to understanding the ecology and evolutionary stability of these mutualisms. We surveyed multiple populations of both Breynia oblongifolia (Phyllanthaceae) and it’s Epicephala pollinators for over two years to determine their phenology and modelled the environmental factors that underpin their interactions. Results: The abundance of flowers and fruits was highly variable and strongly linked to local rainfall and photoperiod. Unlike male flowers and fruits, female flowers were present throughout the entire year, including winter. Fruit abundance was a significant predictor of adult Epicephala activity, suggesting that eggs or early instar larvae diapause within dormant female flowers and emerge as fruits mature. Searches of overwintering female flowers confirmed that many contained pollen and diapausing pollinators. We also observed diapause in Epicephala prior to pupation, finding that 12% (9/78) of larvae emerging from fruits in the autumn entered an extended diapause for 38–48 weeks. The remaining autumn emerging larvae pupated directly without diapause, suggesting a possible bet-hedging strategy. Conclusions: Epicephala appear to use diapause at multiple stages in their lifecycle to survive variable host plant phenology. Furthermore, moth abundance was predicted by the same environmental variables as male flowers, suggesting that moths track flowering through temperature. These adaptations may thereby mitigate against unpredictability in the timing of fruiting and flowering because of variable rainfall. It remains to be seen how widespread egg diapause and pre-pupal diapause may be within Epicephala moths, and, furthermore, to what degree these traits may have facilitated the evolution of these highly diverse mutualisms

Drone-based thermal remote sensing provides an effective new tool for monitoring the abundance of roosting fruit bats

Accurate and precise monitoring of species abundance is essential for determining population trends and responses to environmental change. However, traditional population survey methods can be unreliable and labour-intensive, which complicates the effective conservation and management of many threatened species. We developed a method of using drone-acquired thermal orthomosaics to monitor the abundance of grey-headed flying-foxes (Pteropus poliocephalus) within tree roosts, an IUCN Red Listed species of bat. We assessed the accuracy and precision of this new method and evaluated the performance of four semiautomated methods for counting flying-foxes in thermal orthomosaics, including machine learning and Computer Vision (CV) methods. We found a high concordance between the number of flying-foxes manually counted in drone-acquired thermal imagery and the true abundance of flying-foxes in single roost trees, as obtained from direct on-ground observation. This indicated that the number of flying-foxes observed in thermal imagery accurately reflected the true abundance of flying-foxes. In addition, for thermal orthomosaics of whole roost sites, the number of flying-foxes manually counted was highly repeatable between the same-day drone surveys and human counters, indicating that this method produced highly precise abundance estimates independent of the identity/experience of human counters. Finally, the number of flying-foxes manually counted in drone-acquired thermal orthomosaics was highly concordant with the counts derived from CV and machine learning-enabled classification techniques. This indicated that accurate and precise measures of colony abundance can be obtained semi-automatically, thus greatly reducing the amount of human effort involved for obtaining abundance estimates. Our method is thus valuable for reliably monitoring the abundance of individuals in flying-fox roosts and will aid in the conservation and management of this globally threatened group of flying-mammals, as well as other homeothermic arboreal-roosting species

Risk of SARS-CoV-2 transmission from humans to bats : an Australian assessment

SARS-CoV-2, the cause of COVID-19, infected over 100 million people globally by February 2021. Reverse zoonotic transmission of SARS-CoV-2 from humans to other species has been documented in pet cats and dogs, big cats and gorillas in zoos, and farmed mink. As SARS-CoV-2 is closely related to known bat viruses, assessment of the potential risk of transmission of the virus from humans to bats, and its subsequent impacts on conservation and public health, is warranted. A qualitative risk assessment was conducted by a multi-disciplinary group to assess this risk in bats in the Australian context, with the aim of informing risk management strategies for human activities involving interactions with bats. The overall risk of SARS-CoV-2 establishing in an Australian bat population was assessed to be Low, however with a High level of uncertainty. The outcome of the assessment indicates that, for the Australian situation where the prevalence of COVID-19 in humans is very low, it is reasonable for research and rehabilitation of bats to continue, provided additional biosecurity measures are applied. Risk assessment is challenging for an emerging disease where information is lacking and the situation is changing rapidly; assessments should be revised if human prevalence or other important factors change significantly. The framework developed here, based on established animal disease risk assessment approaches adapted to assess reverse zoonotic transmission, has potential application to a range of wildlife species and situations

Threatened but not conserved: flying-fox roosting and foraging habitat in Australia

Conservation relies upon a primary understanding of changes in a species' population size, distribution, and habitat use. Bats represent about one in five mammal species in the world, but understanding for most species is poor. For flying-foxes, specifically the 66 Pteropus species globally, 31 are classified as threatened (Vulnerable, Endangered, Critically Endangered) on the IUCN Red List. Flying-foxes typically aggregate in colonies of thousands to hundreds of thousands of individuals at their roost sites, dispersing at sunset to forage on floral resources (pollen, nectar, and fruit) in nearby environments. However, understanding of flying-fox roosting habitat preferences is poor, hindering conservation efforts in many countries. In this study, we used a database of 654 known roost sites of the four flying-fox species that occur across mainland Australia to determine the land-use categories and vegetation types in which roost sites were found. In addition, we determined the land-use categories and vegetation types found within the surrounding 25 km radius of each roost, representing primary foraging habitat. Surprisingly, for the four species most roosts occurred in urban areas (42-59%, n = 4 species) followed by agricultural areas (21-31%). Critically, for the two nationally listed species, only 5.2% of grey-headed and 13.9% of spectacled flying-fox roosts occurred in habitat within protected areas. Roosts have previously been reported to predominantly occur in rainforest, mangrove, wetland, and dry sclerophyll vegetation types. However, we found that only 20-35% of roosts for each of the four species occurred in these habitats. This study shows that flying-fox roosts overwhelmingly occurred within human-modified landscapes across eastern Australia, and that conservation reserves inadequately protect essential habitat of roosting and foraging flying-foxes

Body-size dependent foraging strategies in the Christmas Island flying-fox : implications for seed and pollen dispersal within a threatened island ecosystem

Background: Animals are important vectors for the dispersal of a wide variety of plant species, and thus play a key role in maintaining the health and biodiversity of natural ecosystems. On oceanic islands, flying-foxes are often the only seed dispersers or pollinators. However, many flying-fox populations are currently in decline, particularly those of insular species, and this has consequences for the ecological services they provide. Knowledge of the drivers and the scale of flying-fox movements is important in determining the ecological roles that flying-foxes play on islands. This information is also useful for understanding the potential long-term consequences for forest dynamics resulting from population declines or extinction, and so can aid in the development of evidence-based ecological management strategies. To these ends, we examined the foraging movements, floral resource use, and social interactions of the Critically Endangered Christmas Island flying-fox (Pteropus natalis). Methods: Utilization distributions, using movement-based kernel estimates (MBKE) were generated to determine nightly foraging movements of GPS-tracked P. natalis (n = 24). Generalized linear models (GLMs), linear mixed-effect models (LMMs), and Generalized linear mixed-effects model (GLMMs) were constructed to explain how intrinsic factors (body mass, skeletal size, and sex) affected the extent of foraging movements. In addition, we identified pollen collected from facial and body swabs of P. natalis (n = 216) to determine foraging resource use. Direct observations (n = 272) of foraging P. natalis enabled us to assess the various behaviors used to defend foraging resources. Results: Larger P. natalis individuals spent more time foraging and less time traveling between foraging patches, traveled shorter nightly distances, and had smaller overall foraging ranges than smaller conspecifics. Additionally, larger individuals visited a lower diversity of floral resources. Conclusions: Our findings suggest that smaller P. natalis individuals are the primary vectors of long-distance dispersal of pollen and digested seeds in this species, providing a vital mechanism for maintaining the flow of plant genetic diversity across Christmas Island. Overall, our study highlights the need for more holistic research approaches that incorporate population demographics when assessing a species’ ecological services

Extreme mobility of the world’s largest flying mammals creates key challenges for management and conservation

Effective conservation management of highly mobile species depends upon detailed knowledge of movements of individuals across their range; yet, data are rarely available at appropriate spatiotemporal scales. Flying-foxes (Pteropus spp.) are large bats that forage by night on floral resources and rest by day in arboreal roosts that may contain colonies of many thousands of individuals. They are the largest mammals capable of powered flight, and are highly mobile, which makes them key seed and pollen dispersers in forest ecosystems. However, their mobility also facilitates transmission of zoonotic diseases and brings them in conflict with humans, and so they require a precarious balancing of conservation and management concerns throughout their Old World range. Here, we analyze the Australia-wide movements of 201 satellite-tracked individuals, providing unprecedented detail on the inter-roost movements of three flying-fox species: Pteropus alecto, P. poliocephalus, and P. scapulatus across jurisdictions over up to 5 years

The capacity of refugia for conservation planning under climate change

Refugia – areas that may facilitate the persistence of species during large-scale, long-term climatic change – are increasingly important for conservation planning. There are many methods for identifying refugia, but the ability to quantify their potential for facilitating species persistence (ie their “capacity”) remains elusive. We propose a flexible framework for prioritizing future refugia, based on their capacity. This framework can be applied through various modeling approaches and consists of three steps: (1) definition of scope, scale, and resolution; (2) identification and quantification; and (3) prioritization for conservation. Capacity is quantified by multiple indicators, including environmental stability, microclimatic heterogeneity, size, and accessibility of the refugium. Using an integrated, semi-mechanistic modeling technique, we illustrate how this approach can be implemented to identify refugia for the plant diversity of Tasmania, Australia. The highest- capacity climate-change refugia were found primarily in cool, wet, and topographically complex environments, several of which we identify as high priorities for biodiversity conservation and management