Seasonal challenges of tropical bats (Rousettus aegyptiacus) in temperate zones

Egyptian fruit bats (Rousettus aegyptiacus) manage to survive and flourish in a large geographic range despite the variability of natural and anthropogenic conditions in this range. To examine the challenges faced by free-ranging R. aegyptiacus living at the northern edge of their distribution, we performed a retrospective analysis of ~1500 clinical cases reported by a bat rescue NGO over 25 months, from all over Israel. All cases of injured or stranded bats were evaluated and categorized according to date, place, sex, age, and etiology of the morbidity. The analysis of the data showed an increase in all types of morbidity during the wintertime, with more than twice the number of cases in comparison with the summertime, over two consecutive years. Moreover, we found that the number of abandoned pups peaks during spring till autumn when adult morbidity is minimal. We characterize two prominent types of previously undescribed morbidity in R. aegyptiacus, one in the form of bacterial illness, and the other associated with feet deformation which affects bats in addition to major anthropogenic-related threats related to synanthropic predators. We analyze the reasons driving winter morbidity and conclude that winter weather and specifically low temperature best explains this morbidity. We hypothesize that R. aegyptiacus, a fruit-bat of tropical origin is facing major seasonal difficulties near the northern edge of its distribution, probably limiting its further spread northward.

Reproduction, seasonal morphology, and juvenile growth in three Malagasy fruit bats

The island nation of Madagascar is home to three endemic species of Old World Fruit Bat in the family Pteropodidae: Pteropus rufus, Eidolon dupreanum, and Rousettus madagascariensis, all three of which are IUCN Red Listed under some category of threat. To inform conservation efforts to model population viability for these threatened species, as well understand the mechanisms underpinning persistence of several potentially zoonotic pathogens hosted by these bats, we here define the seasonal limits of a staggered annual birth pulse across the three species. Our field studies in central-eastern Madagascar indicate that this annual birth pulse takes place in September/October for P. rufus, November for E. dupreanum, and December for R. madagascariensis. Juvenile development periods vary across the three Malagasy pteropodids, resulting in near-synchronous weaning of pups for all species in late January-February at the height of the fruiting season for Madagascar, a pattern characteristic of most mammalian frugivores on the island. We here document the size range in morphological traits for the three Malagasy fruit bat species; these traits span the range of those known for pteropodids more broadly, with P. rufus and E. dupreanum among the larger of recorded species and R. madagascariensis among the smaller. All three species demonstrate subtle sexual dimorphism in observed traits with larger-bodied males vs. females. We explore seasonal variation in adult body condition by comparing observed body mass with body mass predicted by forearm length, demonstrating that pregnant females add weight during staggered gestation periods and males lose weight during the nutritionally-deficit Malagasy winter. Finally, we quantify forearm, tibia, and ear length growth rates in juvenile bats, demonstrating both faster growth and more protracted development times for the largest P. rufus species. The longer development period for the already-threatened P. rufus further jeopardizes this species' conservation status as human hunting of bats for subsistence is particularly detrimental to population viability during reproductive periods. The more extreme seasonal variation in the mass to forearm relationship for P. rufus may also modulate immune function, an important consideration given these bats' roles as reservoir hosts for several high profile viral families known to cause severe disease in humans. Our work highlights the importance of longitudinal field studies in collecting critical data for mammalian conservation efforts and human public health alike.

Hearing, echolocation, and beam steering from day 0 in tongue-clicking bats

Little is known about the ontogeny of lingual echolocation. We examined the echolocation development of Rousettus aegyptiacus , the Egyptian fruit bat, which uses rapid tongue movements to produce hyper-short clicks and steer the beam's direction. We recorded from day 0 to day 35 postbirth and assessed hearing and beam-steering abilities. On day 0, R. aegyptiacus pups emit isolation calls and hyper-short clicks in response to acoustic stimuli, demonstrating hearing. Auditory brainstem response recordings show that pups are sensitive to pure tones of the main hearing range of adult Rousettus and to brief clicks. Newborn pups produced clicks in the adult paired pattern and were able to use their tongues to steer the sonar beam. As they aged, pups produced click pairs faster, converging with adult intervals by age of first flights (7–8 weeks). In contrast with laryngeal bats, Rousettus echolocation frequency and duration are stable through to day 35, but shift by the time pups begin to fly, possibly owing to tongue-diet maturation effects. Furthermore, frequency and duration shift in the opposite direction of mammalian laryngeal vocalizations. Rousettus lingual echolocation thus appears to be a highly functional sensory system from birth and follows a different ontogeny from that of laryngeal bats.

Dispersal Patterns, Mating Strategy and Genetic Diversity in the Short Nosed Fruit Bat Cynopterus sphinx (Chiroptera: Pteropodidae) in Southern India

The short-nosed fruit bat, Cynopterus sphinx is a common plant-visiting bat that is widely distributed throughout the Indo-Malayan region. In this chapter, we discuss the dispersal patterns, mating strategy and genetic diversity in the short-nosed fruit bat C. sphinx. We used a broad-range of techniques, including mark-recapture, radio-telemetry and molecular biology analyses. Our studies uncovered unique aspects of the dispersal, mating system and genetic diversity of these bats. Both the sexes of C. sphinx were found to disperse completely from the natal harems before subadult stage and young female C. sphinx become members of a harem much earlier than their male counterparts. The nonharem males are reproductively active, gain access to harem females and sire more offspring in July–August breeding season than March–April breeding season and presumably obtain some reproductive success. Our molecular study shows that considerable genetic diversity was observed in this species from different zonal populations, possibly due to complete dispersal of juveniles of both the sexes from their natal groups and gene flow between the zones. All these studies suggest not only a predictive framework for future studies, but also the use of these data in the management and meaningful conservation of this species.

Carollia perspicillata: A Small Bat with Tremendous Translational Potential for Studies of Brain Aging and Neurodegeneration

As the average human lifespan lengthens, the impact of neurodegenerative disease increases, both on the individual suffering neurodegeneration and on the community that supports those individuals. Studies aimed at understanding the mechanisms of neurodegeneration have relied heavily on observational studies of humans and experimental studies in animals, such as mice, in which aspects of brain structure and function can be manipulated to target mechanistic steps. An animal model whose brain is structurally closer to the human brain, that lives much longer than rodents, and whose husbandry is practical may be valuable for mechanistic studies that cannot readily be conducted in rodents. To demonstrate that the long-lived Seba’s short-tailed fruit bat, Carollia perspicillata, may fit this role, we used immunohistochemical labeling for NeuN and three calcium-binding proteins, calretinin, parvalbumin, and calbindin, to define hippocampal formation anatomy. Our findings demonstrate patterns of principal neuron organization that resemble primate and human hippocampal formation and patterns of calcium-binding protein distribution that help to define subregional boundaries. Importantly, we present evidence for a clear prosubiculum in the bat brain that resembles primate prosubiculum. Based on the similarities between bat and human hippocampal formation anatomy, we suggest that Carollia has unique advantages for the study of brain aging and neurodegeneration. A captive colony of Carollia allows age tracking, diet and environment control, pharmacological manipulation, and access to behavioral, physiological, anatomical, and molecular evaluation.

Effects of Overexpression of the Egyptian Fruit Bat Innate Immune Genes on Filovirus Infections in the Host Cells

Bats constitute a large and diverse group of mammals with unique characteristics. One of these is the ability of bats to maintain various pathogens, particularly viruses, without evidence of disease. The innate immune system has been implicated as one of the important components involved in this process. However, in contrast to the human innate immune system, little data is available for bats. In the present study we generated 23 fusion constructs of innate immune genes of Egyptian fruit bat (Rousettus aegyptiacus) with mCherry as a fluorescent reporter. We evaluated the effects of overexpressing these genes on the replication of Marburg and Ebola viruses in the Egyptian fruit bat cell line R06EJ. Both viruses were substantially inhibited by overexpression of type I, II and III interferons, as well as by DDX58 (RIG-I), IFIH1, and IRF1. Our observations suggest that the broad antiviral activity of these genes reported previously in human cells is conserved in Egyptian fruit bats and these possess anti-filovirus activities that may contribute to the efficient virus clearance.

Full genome Nobecovirus sequences from Malagasy fruit bats define a unique evolutionary history for this coronavirus clade

Bats are natural reservoirs for both Alpha- and Betacoronaviruses and the hypothesized original hosts of five of seven known zoonotic coronaviruses. To date, the vast majority of bat coronavirus research has been concentrated in Asia, though coronaviruses are globally distributed; indeed, SARS-CoV and SARS-CoV-2-related Betacoronaviruses in the subgenus Sarbecovirus have been identified circulating in Rhinolophid bats in both Africa and Europe, despite the relative dearth of surveillance in these regions. As part of a long-term study examining the dynamics of potentially zoonotic viruses in three species of endemic Madagascar fruit bat (Pteropus rufus, Eidolon dupreanum, Rousettus madagascariensis), we carried out metagenomic Next Generation Sequencing (mNGS) on urine, throat, and fecal samples obtained from wild-caught individuals. We report detection of RNA derived from Betacoronavirus subgenus Nobecovirus in fecal samples from all three species and describe full genome sequences of novel Nobecoviruses in P. rufus and R. madagascariensis. Phylogenetic analysis indicates the existence of five distinct Nobecovirus clades, one of which is defined by the highly divergent sequence reported here from P. rufus bats. Madagascar Nobecoviruses derived from P. rufus and R. madagascariensis demonstrate, respectively, Asian and African phylogeographic origins, mirroring those of their fruit bat hosts. Bootscan recombination analysis indicates significant selection has taken place in the spike, nucleocapsid, and NS7 accessory protein regions of the genome for viruses derived from both bat hosts. Madagascar offers a unique phylogeographic nexus of bats and viruses with both Asian and African phylogeographic origins, providing opportunities for unprecedented mixing of viral groups and, potentially, recombination. As fruit bats are handled and consumed widely across Madagascar for subsistence, understanding the landscape of potentially zoonotic coronavirus circulation is essential for mitigation of future zoonotic threats.

Seasonal Activity of Fruit Bats in a Monoculture Rubber and Oil Palm Plantation in the Southern Philippines

The increasing expansion of monoculture plantations poses a major threat to Asian tropical biodiversity. Yet, in many countries such as the Philippines, the ability of species to persist within plantations has never been explored. We studied the seasonal activity and response of fruit bats in two types of monocultural plantations (rubber and oil palm) in the Southern Philippines from 2016–17 for 12 months. Our mist-netting and monitoring data showed that both plantations can support cosmopolitan species of fruit bats (Cynopterus brachyotis, Eonycteris spelaea, Macroglossus minimus, Ptenochirus jagori, and Rousettus amplexicaudatus), yet a significant variation in the abundance and guild distribution between plantations was observed. Rubber hosted a higher bat abundance than oil palm, which may be influenced by better habitat structure of the matrix (e.g., presence of orchard and fruit plantations) and practices occurring in the rubber plantation. We find that, among seasonal climatic variables, temperature showed significant negative effects on fruit bat abundance. Our results suggest that although monoculture plantations host low diversity (i.e., richness and endemism) they still support generalists which are still ecologically important species. Furthermore, wildlife-friendly commercial plantation practices could both enhance economic growth and biodiversity conservation in the Philippines. Our data both provide the potential for long-term monitoring in the Philippines and highlight the need for more comprehensive monitoring of other bat functional groups and their ability to transverse plantations to provide a more in-depth understanding of the roles and impacts of plantations and other land-use changes.