SciCombinator

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Concept: Bat

291

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

214

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

196

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

176

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

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

167

Gammaherpesviruses (γHVs) are generally considered host specific and to have codiverged with their hosts over millions of years. This tenet is challenged here by broad-scale phylogenetic analysis of two viral genes using the largest sample of mammalian γHVs to date, integrating for the first time bat γHV sequences available from public repositories and newly generated viral sequences from two vampire bat species (Desmodus rotundus and Diphylla ecaudata). Bat and primate viruses frequently represented deep branches within the supported phylogenies and clustered among viruses from distantly related mammalian taxa. Following evolutionary scenario testing, we determined the number of host-switching and cospeciation events. Cross-species transmissions have occurred much more frequently than previously estimated, and most of the transmissions were attributable to bats and primates. We conclude that the evolution of the Gammaherpesvirinae subfamily has been driven by both cross-species transmissions and subsequent cospeciation within specific viral lineages and that the bat and primate orders may have potentially acted as superspreaders to other mammalian taxa throughout evolutionary history.

Concepts: Evolution, Biology, Species, Mammal, Primate, Cladistics, Bat, Vampire bat

166

Echolocating bats construct an auditory world sequentially by analyzing successive pulse-echo pairs. Many other mammals rely upon a visual world, acquired by sequential foveal fixations connected by visual gaze saccades. We investigated the scanning behavior of bats and compared it to visual scanning. We assumed that each pulse-echo pair evaluation corresponds to a foveal fixation and that sonar beam movements between pulses can be seen as acoustic gaze saccades. We used a two-dimensional 16 microphone array to determine the sonar beam direction of succeeding pulses and to characterize the three dimensional scanning behavior in the common pipistrelle bat (Pipistrellus pipistrellus) flying in the field. We also used variations of signal amplitude of single microphone recordings as indicator for scanning behavior in open space. We analyzed 33 flight sequences containing more than 700 echolocation calls to determine bat positions, source levels, and beam aiming. When searching for prey and orienting in space, bats moved their sonar beam in all directions, often alternately back and forth. They also produced sequences with irregular or no scanning movements. When approaching the array, the scanning movements were much smaller and the beam was moved over the array in small steps. Differences in the scanning pattern at various recording sites indicated that the scanning behavior depended on the echolocation task that was being performed. The scanning angles varied over a wide range and were often larger than the maximum angle measurable by our array. We found that echolocating bats use a “saccade and fixate” strategy similar to vision. Through the use of scanning movements, bats are capable of finding and exploring targets in a wide search cone centered along flight direction.

Concepts: Dimension, Sequence, Animal echolocation, Bat, Microbat, Common Pipistrelle, Pipistrellus, Soprano Pipistrelle

165

Laryngeally echolocating bats avoid self-deafening (forward masking) by separating pulse and echo either in time using low duty cycle (LDC) echolocation, or in frequency using high duty cycle (HDC) echolocation. HDC echolocators are specialized to detect fluttering targets in cluttered environments. HDC echolocation is found only in the families Rhinolophidae and Hipposideridae in the Old World and in the New World mormoopid, Pteronotus parnellii. Here we report that the hipposiderid Coelops frithii, ostensibly an HDC bat, consistently uses an LDC echolocation strategy whether roosting, flying, or approaching a fluttering target rotating at 50 to 80 Hz. We recorded the echolocation calls of free-flying C. frithii in the field in various situations, including presenting bats with a mechanical fluttering target. The echolocation calls of C. frithii consisted of an initial narrowband component (0.5±0.3 ms, 90.6±2.0 kHz) followed immediately by a frequency modulated (FM) sweep (194 to 113 kHz). This species emitted echolocation calls at duty cycles averaging 7.7±2.8% (n = 87 sequences). Coelops frithii approached fluttering targets more frequently than did LDC bats (C.frithii, approach frequency  = 40.4%, n = 80; Myotis spp., approach frequency  = 0%, n = 13), and at the same frequency as sympatrically feeding HDC species (Hipposideros armiger, approach rate  = 53.3%, n = 15; Rhinolophus monoceros, approach rate  = 56.7%, n = 97). We propose that the LDC echolocation strategy used by C. frithii is derived from HDC ancestors, that this species adjusts the harmonic contents of its echolocation calls, and that it may use both the narrowband component and the FM sweep of echolocations calls to detect fluttering targets.

Concepts: Instrument approach, Ultrasound, Frequency, Hertz, Animal echolocation, Bat, Microbat, Horseshoe bat