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Concept: Bat

298

In this paper more than 50 incidences of bats being captured by spiders are reviewed. Bat-catching spiders have been reported from virtually every continent with the exception of Antarctica (∼90% of the incidences occurring in the warmer areas of the globe between latitude 30° N and 30° S). Most reports refer to the Neotropics (42% of observed incidences), Asia (28.8%), and Australia-Papua New Guinea (13.5%). Bat-catching spiders belong to the mygalomorph family Theraphosidae and the araneomorph families Nephilidae, Araneidae, and Sparassidae. In addition to this, an attack attempt by a large araneomorph hunting spider of the family Pisauridae on an immature bat was witnessed. Eighty-eight percent of the reported incidences of bat catches were attributable to web-building spiders and 12% to hunting spiders. Large tropical orb-weavers of the genera Nephila and Eriophora in particular have been observed catching bats in their huge, strong orb-webs (of up to 1.5 m diameter). The majority of identifiable captured bats were small aerial insectivorous bats, belonging to the families Vespertilionidae (64%) and Emballonuridae (22%) and usually being among the most common bat species in their respective geographic area. While in some instances bats entangled in spider webs may have died of exhaustion, starvation, dehydration, and/or hyperthermia (i.e., non-predation death), there were numerous other instances where spiders were seen actively attacking, killing, and eating the captured bats (i.e., predation). This evidence suggests that spider predation on flying vertebrates is more widespread than previously assumed.

Concepts: Bat, Spider, Mygalomorphae, Microbat, Orb-weaver spider, Tarantula, Araneomorphae, Vesper bat

224

The remarkable maneuverability of flying animals results from precise movements of their highly specialized wings. Bats have evolved an impressive capacity to control their flight, in large part due to their ability to modulate wing shape, area, and angle of attack through many independently controlled joints. Bat wings, however, also contain many bones and relatively large muscles, and thus the ratio of bats' wing mass to their body mass is larger than it is for all other extant flyers. Although the inertia in bat wings would typically be associated with decreased aerial maneuverability, we show that bat maneuvers challenge this notion. We use a model-based tracking algorithm to measure the wing and body kinematics of bats performing complex aerial rotations. Using a minimal model of a bat with only six degrees of kinematic freedom, we show that bats can perform body rolls by selectively retracting one wing during the flapping cycle. We also show that this maneuver does not rely on aerodynamic forces, and furthermore that a fruit fly, with nearly massless wings, would not exhibit this effect. Similar results are shown for a pitching maneuver. Finally, we combine high-resolution kinematics of wing and body movements during landing and falling maneuvers with a 52-degree-of-freedom dynamical model of a bat to show that modulation of wing inertia plays the dominant role in reorienting the bat during landing and falling maneuvers, with minimal contribution from aerodynamic forces. Bats can, therefore, use their wings as multifunctional organs, capable of sophisticated aerodynamic and inertial dynamics not previously observed in other flying animals. This may also have implications for the control of aerial robotic vehicles.

Concepts: Insect, Mass, Force, Classical mechanics, Bat, Flight, Wing, Flying and gliding animals

213

The need to develop effective management strategies for insectivorous bat populations requires an understanding of factors influencing habitat use. Availability of pest prey, such as mosquitoes is likely to be one such factor. To assess whether this is the case, we radio-tracked Vespadelus vulturnus Thomas (little forest bat), a predator of Aedes vigilax Skuse (saltmarsh mosquito), in saltmarsh and adjacent coastal swamp forest during periods of high and low Ae. vigilax abundance. When mosquito abundance in structurally-open saltmarsh was similar to the more cluttered coastal swamp forest, use of saltmarsh by V. vulturnus was disproportionately greater than its availability, with saltmarsh selected preferentially for foraging. However, at times of low Ae. vigilax abundance in saltmarsh, use of saltmarsh by V. vulturnus was reduced and all habitats were used in proportion to availability in the study area. This is the first radio-tracking study to demonstrate a shift in foraging range by an insectivorous bat species correlated with fluctuations in the distribution and abundance of a particular prey resource. The shift in foraging range by V. vulturnus, corresponding with a spatio-temporal variation in abundance of Ae. vigilax highlights the importance of mosquitoes as a dietary item. Broadscale pest control of Ae. vigilax may have ecological implications for the diet and habitat use of V. vulturnus. An adaptive management approach is proposed, whereby careful monitoring of insectivorous bat populations is recommended before and after any application of broadscale mosquito control measures. We also suggest a precautionary approach is taken such that broadscale control of mosquitoes avoids the lactation period of bats, a time when their energetic demands are greatest and when there is reduced risk of contracting mosquito-borne diseases transmitted by Ae. vigilax.

Concepts: Insect, Mosquito, Animal echolocation, Aedes, Bat, Mosquito control, Microbat, Vespadelus

209

Since the emergence of Severe Acute Respiratory Syndrome Coronavirus (SARS-CoV) and Middle East Respiratory Syndrom Coronavirus (MERS-CoV) it has become increasingly clear that bats are important reservoirs of CoVs. Despite this, only 6% of all CoV sequences in GenBank are from bats. The remaining 94% largely consist of known pathogens of public health or agricultural significance, indicating that current research effort is heavily biased towards describing known diseases rather than the ‘pre-emergent’ diversity in bats. Our study addresses this critical gap, and focuses on resource poor countries where the risk of zoonotic emergence is believed to be highest. We surveyed the diversity of CoVs in multiple host taxa from twenty countries to explore the factors driving viral diversity at a global scale. We identified sequences representing 100 discrete phylogenetic clusters, ninety-one of which were found in bats, and used ecological and epidemiologic analyses to show that patterns of CoV diversity correlate with those of bat diversity. This cements bats as the major evolutionary reservoirs and ecological drivers of CoV diversity. Co-phylogenetic reconciliation analysis was also used to show that host switching has contributed to CoV evolution, and a preliminary analysis suggests that regional variation exists in the dynamics of this process. Overall our study represents a model for exploring global viral diversity and advances our fundamental understanding of CoV biodiversity and the potential risk factors associated with zoonotic emergence.

Concepts: Epidemiology, Biodiversity, Conservation biology, Evolution, Ecology, Severe acute respiratory syndrome, Mathematical analysis, Bat

208

Bats are sources of high viral diversity and high-profile zoonotic viruses worldwide. Although apparently not pathogenic in their reservoir hosts, some viruses from bats severely affect other mammals, including humans. Examples include severe acute respiratory syndrome coronaviruses, Ebola and Marburg viruses, and Nipah and Hendra viruses. Factors underlying high viral diversity in bats are the subject of speculation. We hypothesize that flight, a factor common to all bats but to no other mammals, provides an intensive selective force for coexistence with viral parasites through a daily cycle that elevates metabolism and body temperature analogous to the febrile response in other mammals. On an evolutionary scale, this host-virus interaction might have resulted in the large diversity of zoonotic viruses in bats, possibly through bat viruses adapting to be more tolerant of the fever response and less virulent to their natural hosts.

Concepts: Bacteria, Evolution, Severe acute respiratory syndrome, Mammal, Fever, Bat, Viral hemorrhagic fever, Natural reservoir

208

Hantaviruses are among the most important zoonotic pathogens of humans and the subject of heightened global attention. Despite the importance of hantaviruses for public health, there is no consensus on their evolutionary history and especially the frequency of virus-host co-divergence versus cross-species virus transmission. Documenting the extent of hantavirus biodiversity, and particularly their range of mammalian hosts, is critical to resolving this issue. Here, we describe four novel hantaviruses (Huangpi virus, Lianghe virus, Longquan virus, and Yakeshi virus) sampled from bats and shrews in China, and which are distinct from other known hantaviruses. Huangpi virus was found in Pipistrellus abramus, Lianghe virus in Anourosorex squamipes, Longquan virus in Rhinolophus affinis, Rhinolophus sinicus, and Rhinolophus monoceros, and Yakeshi virus in Sorex isodon, respectively. A phylogenetic analysis of the available diversity of hantaviruses reveals the existence of four phylogroups that infect a range of mammalian hosts, as well as the occurrence of ancient reassortment events between the phylogroups. Notably, the phylogenetic histories of the viruses are not always congruent with those of their hosts, suggesting that cross-species transmission has played a major role during hantavirus evolution and at all taxonomic levels, although we also noted some evidence for virus-host co-divergence. Our phylogenetic analysis also suggests that hantaviruses might have first appeared in Chiroptera (bats) or Soricomorpha (moles and shrews), before emerging in rodent species. Overall, these data indicate that bats are likely to be important natural reservoir hosts of hantaviruses.

Concepts: Evolution, Microbiology, Species, Mammal, Rodent, Bat, Zoonosis, Natural reservoir

203

ABSTRACT A new human coronavirus (hCoV-EMC) has emerged very recently in the Middle East. The clinical presentation resembled that of the severe acute respiratory syndrome (SARS) as encountered during the epidemic in 2002/2003. In both cases, acute renal failure was observed in humans. HCoV-EMC is a member of the same virus genus as SARS-CoV but constitutes a sister species. Here we investigated whether it might utilize angiotensin-converting enzyme 2 (ACE2), the SARS-CoV receptor. Knowledge of the receptor is highly critical because the restriction of the SARS receptor to deep compartments of the human respiratory tract limited the spread of SARS. In baby hamster kidney (BHK) cells, lentiviral transduction of human ACE2 (hACE2) conferred permissiveness and replication for SARS-CoV but not for hCoV-EMC. Monkey and human kidney cells (LLC-MK2, Vero, and 769-P) and swine kidney cells were permissive for both viruses, but only SARS-CoV infection could be blocked by anti-hACE2 antibody and could be neutralized by preincubation of virus with soluble ACE2. Our data show that ACE2 is neither necessary nor sufficient for hCoV-EMC replication. Moreover, hCoV-EMC, but not SARS-CoV, replicated in cell lines from Rousettus, Rhinolophus, Pipistrellus, Myotis, and Carollia bats, representing four major chiropteran families from both suborders. As human CoV normally cannot replicate in bat cells from different families, this suggests that hCoV-EMC might use a receptor molecule that is conserved in bats, pigs, and humans, implicating a low barrier against cross-host transmission. IMPORTANCE  A new human coronavirus (hCoV) emerged recently in the Middle East. The disease resembled SARS (severe acute respiratory syndrome), causing a fatal epidemic in 2002/2003. Coronaviruses have a reservoir in bats and because this novel virus is related to SARS-CoV, we investigated whether it might replicate in bat cells and use the same receptor (angiotensin-converting enzyme 2 [ACE2]). This knowledge is highly critical, because the SARS-CoV receptor influenced pathology, and its localization in the deep respiratory tract is thought to have restricted the transmissibility of SARS. Our data show that hCoV-EMC does not need the SARS-CoV receptor to infect human cells. Moreover, the virus is capable of infecting human, pig, and bat cells. This is remarkable, as human CoVs normally cannot replicate in bat cells as a consequence of host adaptation. Our results implicate that the new virus might use a receptor that is conserved between bats, pigs and humans suggesting a low barrier against cross-host transmission.

Concepts: Protein, Virus, Infection, Severe acute respiratory syndrome, Mammal, Primate, Bat, Coronavirus

172

Schemes designed to make farming landscapes less hostile to wildlife have been questioned because target taxa do not always respond in the expected manner. Microbats are often overlooked in this process, yet persist in agricultural landscapes and exert top-down control of crop pests. We investigated the relationship between microbats and measures commonly incorporated into agri-environment schemes, to derive management recommendations for their ongoing conservation. We used acoustic detectors to quantify bat species richness, activity, and feeding in 32 linear remnants and adjacent fields across an agricultural region of New South Wales, Australia. Nocturnal arthropods were simultaneously trapped using black-light traps. We recorded 91,969 bat calls, 17,277 of which could be attributed to one of the 13 taxa recorded, and 491 calls contained feeding buzzes. The linear remnants supported higher bat activity than the fields, but species richness and feeding activity did not significantly differ. We trapped a mean 87.6 g (±17.6 g SE) of arthropods per night, but found no differences in biomass between land uses. Wider linear remnants with intact native vegetation supported more bat species, as did those adjacent to unsealed, as opposed to sealed roads. Fields of unimproved native pastures, with more retained scattered trees and associated hollows and logs, supported the greatest bat species richness and activity. We conclude that the juxtaposition of linear remnants of intact vegetation and scattered trees in fields, coupled with less-intensive land uses such as unimproved pastures will benefit bat communities in agricultural landscapes, and should be incorporated into agri-environment schemes. In contrast, sealed roads may act as a deterrent. The “wildlife friendly farming” vs “land sparing” debate has so far primarily focussed on birds, but here we have found evidence that the integration of both approaches could particularly benefit bats.

Concepts: Biodiversity, Conservation biology, Agriculture, Insect, Bat, Microbat, Landscape, Bats

172

Bats are among the most gregarious and vocal mammals, with some species demonstrating a diverse repertoire of syllables under a variety of behavioral contexts. Despite extensive characterization of big brown bat (Eptesicus fuscus) biosonar signals, there have been no detailed studies of adult social vocalizations. We recorded and analyzed social vocalizations and associated behaviors of captive big brown bats under four behavioral contexts: low aggression, medium aggression, high aggression, and appeasement. Even limited to these contexts, big brown bats possess a rich repertoire of social vocalizations, with 18 distinct syllable types automatically classified using a spectrogram cross-correlation procedure. For each behavioral context, we describe vocalizations in terms of syllable acoustics, temporal emission patterns, and typical syllable sequences. Emotion-related acoustic cues are evident within the call structure by context-specific syllable types or variations in the temporal emission pattern. We designed a paradigm that could evoke aggressive vocalizations while monitoring heart rate as an objective measure of internal physiological state. Changes in the magnitude and duration of elevated heart rate scaled to the level of evoked aggression, confirming the behavioral state classifications assessed by vocalizations and behavioral displays. These results reveal a complex acoustic communication system among big brown bats in which acoustic cues and call structure signal the emotional state of a caller.

Concepts: Psychology, Sociology, Mammal, Acoustics, Bat, Big brown bat, Little brown bat, Eptesicus

171

The proportion of organisms exposed to warm conditions is predicted to increase during global warming. To better understand how bats might respond to climate change, we aimed to obtain the first data on how use of torpor, a crucial survival strategy of small bats, is affected by temperature in the tropics. Over two mild winters, tropical free-ranging bats (Nyctophilus bifax, 10 g, n = 13) used torpor on 95% of study days and were torpid for 33.5±18.8% of 113 days measured. Torpor duration was temperature-dependent and an increase in ambient temperature by the predicted 2°C for the 21(st) century would decrease the time in torpor to 21.8%. However, comparisons among Nyctophilus populations show that regional phenotypic plasticity attenuates temperature effects on torpor patterns. Our data suggest that heterothermy is important for energy budgeting of bats even under warm conditions and that flexible torpor use will enhance bats' chance of survival during climate change.

Concepts: Tropics, Climate change, Bat, Global warming, Torpor, Hibernation