Reproduction and nutritional stress are risk factors for Hendra virus infection in little red flying foxes (Pteropus scapulatus)

Hendra virus (HeV) is a lethal paramyxovirus which emerged in humans in 1994. Poor understanding of HeV dynamics in Pteropus spp. (flying fox or fruit bat) reservoir hosts has limited our ability to determine factors driving its emergence. We initiated a longitudinal field study of HeV in little red flying foxes (LRFF; Pteropus scapulatus) and examined individual and population risk factors for infection, to determine probable modes of intraspecific transmission. We also investigated whether seasonal changes in host behaviour, physiology and demography affect host-pathogen dynamics. Data showed that pregnant and lactating females had significantly higher risk of infection, which may explain previously observed temporal associations between HeV outbreaks and flying fox birthing periods. Age-specific seroprevalence curves generated from field data imply that HeV is transmitted horizontally via faeces, urine or saliva. Rapidly declining seroprevalence between two field seasons suggests that immunity wanes faster in LRFF than in other flying fox species, and highlights the potentially critical role of this species in interspecific viral persistence. The highest seroprevalence was observed when animals showed evidence of nutritional stress, suggesting that environmental processes that alter flying fox food sources, such as habitat loss and climate change, may increase HeV infection and transmission. These insights into the ecology of HeV in flying fox populations suggest causal links between anthropogenic environmental change and HeV emergence.     

Identifying Hendra virus diversity in pteropid bats

Hendra virus (HeV) causes a zoonotic disease with high mortality that is transmitted to humans from bats of the genus Pteropus (flying foxes) via an intermediary equine host. Factors promoting spillover from bats to horses are uncertain at this time, but plausibly encompass host and/or agent and/or environmental factors. There is a lack of HeV sequence information derived from the natural bat host, as previously sequences have only been obtained from horses or humans following spillover events. In order to obtain an insight into possible variants of HeV circulating in flying foxes, collection of urine was undertaken in multiple flying fox roosts in Queensland, Australia. HeV was found to be geographically widespread in flying foxes with a number of HeV variants circulating at the one time at multiple locations, while at times the same variant was found circulating at disparate locations. Sequence diversity within variants allowed differentiation on the basis of nucleotide changes, and hypervariable regions in the genome were identified that could be used to differentiate circulating variants. Further, during the study, HeV was isolated from the urine of flying foxes on four occasions from three different locations. The data indicates that spillover events do not correlate with particular HeV isolates, suggesting that host and/or environmental factors are the primary determinants of bat-horse spillover. Thus future spillover events are likely to occur, and there is an on-going need for effective risk management strategies for both human and animal health.     

Climate Change Could Increase the Geographic Extent of Hendra Virus Spillover Risk

Disease risk mapping is important for predicting and mitigating impacts of bat-borne viruses, including Hendra virus (Paramyxoviridae:Henipavirus), that can spillover to domestic animals and thence to humans. We produced two models to estimate areas at potential risk of HeV spillover explained by the climatic suitability for its flying fox reservoir hosts, Pteropus alecto and P. conspicillatus. We included additional climatic variables that might affect spillover risk through other biological processes (such as bat or horse behaviour, plant phenology and bat foraging habitat). Models were fit with a Poisson point process model and a log-Gaussian Cox process. In response to climate change, risk expanded southwards due to an expansion of P. alecto suitable habitat, which increased the number of horses at risk by 175–260% (110,000–165,000). In the northern limits of the current distribution, spillover risk was highly uncertain because of model extrapolation to novel climatic conditions. The extent of areas at risk of spillover from P. conspicillatus was predicted shrink. Due to a likely expansion of P. alecto into these areas, it could replace P. conspicillatus as the main HeV reservoir. We recommend: (1) HeV monitoring in bats, (2) enhancing HeV prevention in horses in areas predicted to be at risk, (3) investigate and develop mitigation strategies for areas that could experience reservoir host replacements.     

Coexistence and Conflict between the Island Flying fox (<Emphasis Type="Italic">Pteropus hypomelanus</Emphasis>) and Humans on Tioman Island,Peninsular Malaysia

As tropical landscapes become increasingly human-dominated, conflicts between people and wildlife threaten ecological processes. Old World fruit bats such as flying foxes are especially susceptible to extinction risk because there is low interest in their conservation, particularly when they are considered pests. In order to arrest fruit bat declines, there is an urgent need to understand human-bat conflict and its implications. On a tropical island in Peninsular Malaysia, we conducted a questionnaire survey to investigate coexistence between people and the island flying fox (Pteropus hypomelanus). Among 119 respondents, knowledge of ecosystem services provided by flying foxes was extremely low. Most respondents held negative attitudes towards the bats, and older male locals were more likely to support killing them. This was also true for older owners of fruit trees who derived income from selling fruit, and experienced flying fox raids. Our results can be used to design appropriate interventions to support conservation efforts, and has important implications for managing conflicts between humans and synanthropic wildlife.     

Spatial expansions and travelling waves of rabies in vampire bats

A major obstacle to anticipating the cross-species transmission of zoonotic diseases and developing novel strategies for their control is the scarcity of data informing how these pathogens circulate within natural reservoir populations. Vampire bats are the primary reservoir of rabies in Latin America, where the disease remains among the most important viral zoonoses affecting humans and livestock. Unpredictable spatiotemporal dynamics of rabies within bat populations have precluded anticipation of outbreaks and undermined widespread bat culling programs. By analysing 1146 vampire bat-transmitted rabies (VBR) outbreaks in livestock across 12 years in Peru, we demonstrate that viral expansions into historically uninfected zones have doubled the recent burden of VBR. Viral expansions are geographically widespread, but severely constrained by high elevation peaks in the Andes mountains. Within Andean valleys, invasions form wavefronts that are advancing towards large, unvaccinated livestock populations that are heavily bitten by bats, which together will fuel high transmission and mortality. Using spatial models, we forecast the pathways of ongoing VBR epizootics across heterogeneous landscapes. These results directly inform vaccination strategies to mitigate impending viral emergence, reveal VBR as an emerging rather than an enzootic disease and create opportunities to test novel interventions to manage viruses in bat reservoirs.     

Disease Risk Perception and Safety Practices: A Survey of Australian Flying Fox Rehabilitators

Interactions with flying foxes pose disease transmission risks to volunteer rehabilitators (carers) who treat injured, ill, and orphaned bats. In particular, Australian bat lyssavirus (ABLV) can be transmitted directly from flying foxes to humans in Australia. Personal protective equipment (PPE) and rabies vaccination can be used to protect against lyssavirus infection. During May and June 2014, active Australian flying fox carers participated in an online survey (SOAR: Survey Of Australian flying fox Rehabilitators) designed to gather demographic data, assess perceptions of disease risk, and explore safety practices. Responses to open-ended questions were analysed thematically. A logistic regression was performed to assess whether rehabilitators’ gender, use of PPE, threat perception, and years of experience predicted variation in their odds of being bitten or scratched. Eligible responses were received from 122 rehabilitators located predominantly on the eastern coast of Australia. Eighty-four percent of respondents were female. Years of experience ranged from <1 to 30 years (median 5 years). Respondents were highly educated. All rehabilitators were vaccinated against rabies and 94% received a rabies titre check at least every two years. Sixty-three percent of carers did not perceive viruses in flying foxes as a potential threat to their health, yet 74% of carers reported using PPE when handling flying foxes. Eighty-three percent of rehabilitators had received a flying fox bite or scratch at some point during their career. Carers provide an important community service by rescuing and rehabilitating flying foxes. While rehabilitators in this study have many excellent safety practices, including a 100% vaccination rate against rabies, there is room for improvement in PPE use. We recommend 1) the establishment of an Australia-wide set of guidelines for safety when caring for bats and 2) that the responsible government agencies in Australia support carers who rescue potentially ABLV-infected bats by offering compensation for PPE.     

Seasonal bat activity related to insect emergence at three temperate lakes

Knowledge of aquatic food resources entering terrestrial systems is important for food web studies and conservation planning. Bats, among other terrestrial consumers, often profit from aquatic insect emergence and their activity might be closely related to such events. However, there is a lack of studies which monitor bat activity simultaneously with aquatic insect emergence, especially from lakes. Thus, our aim was to understand the relationship between insect emergence and bat activity, and investigate whether there is a general spatial or seasonal pattern at lakeshores. We assessed whole‐night bat activity using acoustic monitoring and caught emerging and aerial flying insects at three different lakes through three seasons. We predicted that insect availability and seasonality explain the variation in bat activity, independent of the lake size and characteristics. Spatial (between lakes) differences of bat activity were stronger than temporal (seasonal) differences. Bat activity did not always correlate to insect emergence, probably because other factors, such as habitat characteristics, or bats’ energy requirements, play an important role as well. Aerial flying insects explained bat activity better than the emerged aquatic insects in the lake with lowest insect emergence. Bats were active throughout the night with some activity peaks, and the pattern of their activity also differed among lakes and seasons. Lakes are important habitats for bats, as they support diverse bat communities and activity throughout the night and the year when bats are active. Our study highlights that there are spatial and temporal differences in bat activity and its hourly nocturnal pattern, that should be considered when investigating aquatic–terrestrial interactions or designing conservation and monitoring plans.     

Survival and Cause-Specific Mortality of Red Foxes in Agricultural and Urban Areas of Illinois

Abstract: Range expansion and population increase by coyotes (Canis latrans), reduced hunting and trapping, and intensified agricultural practices in the Midwest have altered red fox (Vulpes vulpes) mortality, although relative impacts of these factors are unknown. We examined mortality causes and survival of red foxes in urban and rural agricultural areas of Illinois, using radio telemetry data from 335 foxes (Nov 1996 to May 2002). We used Akaike's Information Criterion to evaluate six survival models for foxes reflecting 1) environmental effects, 2) intrinsic effects, 3) temporal effects, 4) behavioral effects, 5) social effects, and 6) a global model. Environmental and intrinsic models of survival were optimal for adult foxes. Adult foxes with low (0-20%) and high (80-100%) percentages of row crops in their home ranges had higher survival than adults with moderate percentages (40-70%). Heavier adults at capture also survived better. A global model (all covariates) was optimal for juvenile foxes. Higher juvenile survival associated with larger litters, lower body fat, and reduced dispersal time. Yearly survival ranged from 0.18 for rural male juveniles to 0.44 for rural female adults. Adult survival rates (0.35) were 11% higher than juvenile survival rates (0.24). Yearly survival varied for urban foxes due to cyclic outbreaks of sarcoptic mange (Sarcoptes scabei). Thus, summer survival (May-Sep) of urban juveniles ranged from 0.10 (mange present) to 0.83 (no mange recorded). Mange was the most common (45% of all fatalities) source of mortality for urban foxes, followed by road kill (31%). We recorded only 4 mange fatalities (2%) for rural foxes. Rural foxes experienced low hunting mortality (7%) and equivalent road kill and coyote predation fatalities (40% each). Sources of mortality for midwestern foxes have dramatically changed since the 1970s when hunting was the major cause of mortality. Coyote predation has effectively replaced hunting mortality, and cyclic patterns of mange outbreaks in urban fox populations might indicate a dynamic source or sink relationship to surrounding rural fox populations. Absent mange, urban areas might provide refugia for red foxes where coyote populations persist at high densities in rural areas. Managers of sympatric urban and rural wildlife populations must understand survival dynamics influencing the population at the landscape level.     

Hendra virus infection dynamics in Australian fruit bats

Hendra virus is a recently emerged zoonotic agent in Australia. Since first described in 1994, the virus has spilled from its wildlife reservoir (pteropid fruit bats, or 'flying foxes') on multiple occasions causing equine and human fatalities. We undertook a three-year longitudinal study to detect virus in the urine of free-living flying foxes (a putative route of excretion) to investigate Hendra virus infection dynamics. Pooled urine samples collected off plastic sheets placed beneath roosting flying foxes were screened for Hendra virus genome by quantitative RT-PCR, using a set of primers and probe derived from the matrix protein gene. A total of 1672 pooled urine samples from 67 sampling events was collected and tested between 1 July 2008 and 30 June 2011, with 25% of sampling events and 2.5% of urine samples yielding detections. The proportion of positive samples was statistically associated with year and location. The findings indicate that Hendra virus excretion occurs periodically rather than continuously, and in geographically disparate flying fox populations in the state of Queensland. The lack of any detection in the Northern Territory suggests prevalence may vary across the range of flying foxes in Australia. Finally, our findings suggest that flying foxes can excrete virus at any time of year, and that the apparent seasonal clustering of Hendra virus incidents in horses and associated humans (70% have occurred June to October) reflects factors other than the presence of virus. Identification of these factors will strengthen risk minimization strategies for horses and ultimately humans.     

Pollination by the locally endangered island flying fox (Pteropus hypomelanus) enhances fruit production of the economically important durian (Durio zibethinus)

Fruit bats provide valuable pollination services to humans through a unique coevolutionary relationship with chiropterophilous plants. However, chiropterophily in the Old World and the pollination roles of large bats, such as flying foxes (Pteropus spp., Acerodon spp., Desmalopex spp.), are still poorly understood and require further elucidation. Efforts to protect these bats have been hampered by a lack of basic quantitative information on their role as ecosystem service providers. Here, we investigate the role of the locally endangered island flying fox Pteropus hypomelanus in the pollination ecology of durian (Durio zibethinus), an economically important crop in Southeast Asia. On Tioman Island, Peninsular Malaysia, we deployed 19 stations of paired infrared camera and video traps across varying heights at four individual flowering trees in a durian orchard. We detected at least nine species of animal visitors, but only bats had mutualistic interactions with durian flowers. There was a clear vertical stratification in the feeding niches of flying foxes and nectar bats, with flying foxes feeding at greater heights in the trees. Flying foxes had a positive effect on mature fruit set and therefore serve as important pollinators for durian trees. As such, semi‐wild durian trees—particularly tall ones—may be dependent on flying foxes for enhancing reproductive success. Our study is the first to quantify the role of flying foxes in durian pollination, demonstrating that these giant fruit bats may have far more important ecological, evolutionary, and economic roles than previously thought. This has important implications and can aid efforts to promote flying fox conservation, especially in Southeast Asian countries.     

果蝠的婚配制度及繁殖策略

翼手类(Chiroptera)(俗称蝙蝠)分为小蝙蝠亚目(Microchiroptera)和大蝙蝠亚目(Megachiroptera),大蝙蝠又称果蝠或狐蝠,果蝠仅狐蝠科(Pteropodidae)1科188种。深入地了解其独特的婚配行为机制、独特的繁殖发育机制,对有效地开展果蝠的保护工作、合理地控制种群数量有积极意义。本文对果蝠的婚配制度及繁殖策略进行了阐述。     

Taxonomy,distribution, and natural history of flying foxes (Chiroptera,Pteropodidae) in the Mortlock Islands and Chuuk State,Caroline Islands

The taxonomy, biology, and population status of flying foxes (Pteropus spp.) remain little investigated in the Caroline Islands, Micronesia, where multiple endemic taxa occur. Our study evaluated the taxonomic relationships between the flying foxes of the Mortlock Islands (a subgroup of the Carolines) and two closely related taxa from elsewhere in the region, and involved the first ever field study of the Mortlock population. Through a review of historical literature, the name Pteropus pelagicus Kittlitz, 1836 is resurrected to replace the prevailing but younger name Pteropus phaeocephalus Thomas, 1882 for the flying fox of the Mortlocks. On the basis of cranial and external morphological comparisons, Pteropus pelagicus is united taxonomically with Pteropus insularis “Hombron and Jacquinot, 1842” (with authority herein emended to Jacquinot and Pucheran 1853), and the two formerly monotypic species are now treated as subspecies — Pteropus pelagicus pelagicus in the Mortlocks, and Pteropus phaeocephalus insularis on the islands of Chuuk Lagoon and Namonuito Atoll. The closest relative of Pteropus pelagicus is Pteropus tokudae Tate, 1934, of Guam, which is best regarded as a distinct species. Pteropus pelagicus pelagicus is the only known resident bat in the Mortlock Islands, a chain of more than 100 atoll islands with a total land area of <12 km². Based on field observations in 2004, we estimated a population size of 925–1,200 bats, most of which occurred on Satawan and Lukunor Atolls, the two largest and southernmost atolls in the chain. Bats were absent on Nama Island and possibly extirpated from Losap Atoll in the northern Mortlocks. Resident Mortlockese indicated bats were more common in the past, but that the population generally has remained stable in recent years. Most Pteropus phaeocephalus pelagicus roosted alone or in groups of 5–10 bats; a roost of 27 was the largest noted. Diet is comprised of at least eight plant species, with breadfruit (Artocarpus spp.) being a preferred food. Records of females with young (April, July) and pregnant females (July) suggest an extended breeding season. Pteropus pelagicus pelagicus appears most threatened by the prospect of sea level rise associated with global climate change, which has the potential to submerge or reduce the size of atolls in the Mortlocks. Occasional severe typhoons probably temporarily reduce populations on heavily damaged atolls, but hunting and ongoing habitat loss are not current problems for the subspecies.     

Indirect Evidence that Flying Foxes Track Food Resources Among Islands in a Pacific Archipelago

Although flying foxes (fruit bats in the genus Pteropus ) in continental forests often fly between scattered resources, little is known about their ranging behavior among islands. The inhospitable water matrix that surrounds the food patches (islands) in archipelagos may prevent flying foxes from tracking resources as efficiently as their counterparts on larger landmasses do. Our aim in this study was to determine whether the abundance of foraging flying foxes ( Pteropus tonganus ) reflected food availability on islands in the Vava'u archipelago of Tonga, regardless of island size and isolation. Overall, food availability was the strongest determinant of flying fox abundance, and spatial aspects of the islands (land area within 10 km) had only a small influence. Food availability appears to regulate flying fox abundance only when food resources are low, but when food sources are plentiful, flying fox abundance may be high or low. These results provide indirect evidence that flying foxes are able to track food resources efficiently in an archipelago, and the water matrix that surrounds the food patches (islands) is not a strong deterrent for foraging animals.     

Ecological conditions predict the intensity of Hendra virus excretion over space and time from bat reservoir hosts

The ecological conditions experienced by wildlife reservoirs affect infection dynamics and thus the distribution of pathogen excreted into the environment. This spatial and temporal distribution of shed pathogen has been hypothesised to shape risks of zoonotic spillover. However, few systems have data on both long-term ecological conditions and pathogen excretion to advance mechanistic understanding and test environmental drivers of spillover risk. We here analyse three years of Hendra virus data from nine Australian flying fox roosts with covariates derived from long-term studies of bat ecology. We show that the magnitude of winter pulses of viral excretion, previously considered idiosyncratic, are most pronounced after recent food shortages and in bat populations displaced to novel habitats. We further show that cumulative pathogen excretion over time is shaped by bat ecology and positively predicts spillover frequency. Our work emphasises the role of reservoir host ecology in shaping pathogen excretion and provides a new approach to estimate spillover risk.     

Adaptive auditory risk assessment in the dogbane tiger moth when pursued by bats

Moths and butterflies flying in search of mates risk detection by numerous aerial predators; under the cover of night, the greatest threat will often be from insectivorous bats. During such encounters, the toxic dogbane tiger moth, Cycnia tenera uses the received intensity, duration and emission pattern of the bat''s echolocation calls to determine when, and how many, defensive ultrasonic clicks to produce in return. These clicks, which constitute an acoustic startle response, act as warning signals against bats in flight. Using an integrated test of stimulus generalization and dishabituation, here we show that C. tenera is able to discriminate between the echolocation calls characteristic of a bat that has only just detected it versus those of a bat actively in pursuit of it. We also show that C. tenera habituates more profoundly to the former stimulus train (‘early attack’) than to the latter (‘late attack’), even though it was initially equally responsive to both stimuli. Matched sensory and behavioural data indicate that reduced responsiveness reflects habituation and is not merely attributable to sensory adaptation or motor fatigue. In search of mates in the face of bats, C. tenera''s ability to discriminate between attacking bats representing different levels of risk, and to habituate less so to those most dangerous, should function as an adaptive cost–benefit trade-off mechanism in nature.     

The natural history of Hendra and Nipah viruses

Pteropid bats (flying foxes), species of which are the probable natural host of both Hendra and Nipah viruses, occur in overlapping populations from India to Australia. Ecological changes associated with land use and with animal husbandry practices appear most likely to be associated with the emergence of these two agents.     

狐蝠对森林生态系统的作用

翼手目 (Chiroptera)为真正能飞翔的哺乳动物 ,现存 19科 110 7种 ,分别属于小蝙蝠亚目 (Microchiroptera)和大蝙蝠亚目 (Megachiroptera) ;其中大蝙蝠又称旧大陆狐蝠或果蝠 (flyingfox) ,分布在热带和亚热带地区 ,仅狐蝠科 188种 ,我国自然分布有 9种。部分地区因栖息地丧失和过度捕杀导致狐蝠种群数量全球性或地区性下降或灭绝 ;狐蝠通过传播种子或传粉 ,促进森林生态系统的更新和基因交流。因此 ,狐蝠对森林生态系统的稳定、扩散、生物多样性以及衰退森林的恢复有重要作用     

Preference of an insular flying fox for seed figs enhances seed dispersal of a dioecious species

Interactions among multiple species form complex networks of interdependences and are considered primary factors in the generation and maintenance of biodiversity. Pteropodid bats are keystone species that provide important ecosystem services of pollination and seed dispersal in the tropics and subtropics. In this study, we investigated the utilization and preference of food resources by the insular frugivorous flying fox Pteropus dasymallus. We found that fig species constituted the major portion of the diet of the flying fox (94.6%). When foraging, the flying fox preferred seed figs from female trees over gall figs from male trees in functionally dioecious fig species. Germination experiments showed a significantly higher percentage of germination for fig seeds in feces than those from pellets and ripe figs (feces: 80.2%, pellets: 23.4%, ripe figs: 32.9%). Considering the active selection of seed figs and avoidance of gall figs by foraging flying foxes, we suggest that the abundance of seed figs accurately represents food availability for dioecy. This preference for seed figs or viable seeds can effectively promote the survival of pollinating wasps and might reinforce the evolution of dioecism in figs. In addition, the effects of gut passage on seed germination, in combination with the capacity of flying foxes to travel long distances, may substantially contribute to the efficiency of flying foxes as seed dispersers.