York Winter

Absent or low rate of adult neurogenesis in the hippocampus of bats (Chiroptera).

Bats are the only flying mammals and have well developed navigation abilities for 3D-space. Even bats with comparatively small home ranges cover much larger territories than rodents, and long-distance migration by some species is unique among small mammals. Adult proliferation of neurons, i.e., adult neurogenesis, in the dentate gyrus of rodents is thought to play an important role in spatial memory and learning, as indicated by lesion studies and recordings of neurons active during spatial behavior. Assuming a role of adult neurogenesis in hippocampal function, one might expect high levels of adult neurogenesis in bats, particularly among fruit- and nectar-eating bats in need of excellent spatial working memory. The dentate gyrus of 12 tropical bat species was examined immunohistochemically, using multiple antibodies against proteins specific for proliferating cells (Ki-67, MCM2), and migrating and differentiating neurons (Doublecortin, NeuroD). Our data show a complete lack of hippocampal neurogenesis in nine of the species (Glossophaga soricina, Carollia perspicillata, Phyllostomus discolor, Nycteris macrotis, Nycteris thebaica, Hipposideros cyclops, Neoromicia rendalli, Pipistrellus guineensis, and Scotophilus leucogaster), while it was present at low levels in three species (Chaerephon pumila, Mops condylurus and Hipposideros caffer). Although not all antigens were recognized in all species, proliferation activity in the subventricular zone and rostral migratory stream was found in all species, confirming the appropriateness of our methods for detecting neurogenesis. The small variation of adult hippocampal neurogenesis within our sample of bats showed no indication of a correlation with phylogenetic relationship, foraging strategy, type of hunting habitat or diet. Our data indicate that the widely accepted notion of adult neurogenesis supporting spatial abilities needs to be considered carefully. Given their astonishing longevity, certain bat species may be useful subjects to compare adult neurogenesis with other long-living species, such as monkeys and humans, showing low rates of adult hippocampal neurogenesis.

Wing beat kinematics of a nectar-feeding bat, Glossophaga soricina, flying at different flight speeds and Strouhal numbers.

SUMMARY High-speed film analysis showed that the wing beat kinematics in Glossophaga soricina change gradually with increasing flight speed, indicating that there is no sudden gait change at any particular, critical, flight speed. The flight of two adult specimens was studied over a range of flight speeds (1.23-7.52 ms-1) in a 30 m long flight tunnel. During the upstroke in hovering and slow flight there is a tip-reversal or supination of the handwings, which thus produce a backward flick. This backward motion successively disappears at speeds V≈3.2 ms-1, above which the wingtip path becomes more vertical or directed upwards-forwards relative to the still air (the stroke plane angle increasing with flight speed as α=44.8V0.29). We found no correlations between either span ratio SR (the ratio of the wing span on the upstroke to that on the downstroke) and V, or downstroke ratio (the duration of the downstroke divided by the total stroke period) and V. On the other hand, SR decreases significantly with increasing wing beat frequency f, SR∝f-0.40. The Strouhal number (St=f×amplitude/V), a dimensionless parameter describing oscillating flow mechanisms and being a predictor of the unsteadiness of the flow, decreases with the speed as St∝V-1.37. Close to the theoretical minimum power speed (4-6 m s-1) G. soricina operates with a Strouhal number in the region 0.17<St<0.22, which is associated with efficient lift and thrust production. At slower speeds, 3.4-4 m s-1, St is 0.25-0.4, which is still within the favourable region. But at speeds below 3 m s-1 St becomes higher (0.5<St<0.68), indicating that unsteady effects become important, with unfavourable lift and thrust production as a result. Only at these speeds do the bats perform the backward flick during the upstroke, which may produce thrust. This may serve as a compensation in some bats and birds to increase aerodynamic performance.

Foraging in a complex naturalistic environment: capacity of spatial working memory in flower bats.

SUMMARY Memory systems have evolved under selection pressures, such as the need to remember the locations of resources or past events within spatiotemporally dynamic natural environments. The full repertoire of complex behaviours exhibited by animals in dynamic surroundings are, however, difficult to elicit within simply structured laboratory environments. We have developed a computer-controlled naturalistic environment with 64 feeders for simulating dynamic patterns of water or food resource availability (depletion and replenishment) within the laboratory. The combination of feeder and cage remote control permits the automated transfer of animals between cage and test arena and, therefore, high experimental throughput and minimal disturbance to the animals (bats and mice). In the present study, we investigated spatial working memory in nectar-feeding bats (Glossophaga soricina, Phyllostomidae) collecting food from a 64-feeder array. Feeders gave only single rewards within trials so that efficient foraging required bats to avoid depleted locations. Initially, bats tended to revisit feeders (win-stay), but within three trials changed towards a win-shift strategy. The significant avoidance of revisits could not be explained by algorithmic search guiding movement through the array nor by scent cues left by the bats themselves and, thus, the data suggest that bats remembered spatial locations depleted of food. An examination of the recency effect on spatial working memory after bats shifted to a win-shift strategy indicated that bats held more than 40 behaviour actions (feeder visits) in working memory without indication of decay. This result surpasses previous findings for other taxa.

Kinematics of flight and the relationship to the vortex wake of a Pallas' long tongued bat (Glossophaga soricina)

SUMMARY To obtain a full understanding of the aerodynamics of animal flight, the movement of the wings, the kinematics, needs to be connected to the wake left behind the animal. Here the detailed 3D wingbeat kinematics of bats, Glossophaga soricina, flying in a wind tunnel over a range of flight speeds (1–7 m s−1) was determined from high-speed video. The results were compared with the wake geometry and quantitative wake measurements obtained simultaneously to the kinematics. The wingbeat kinematics varied gradually with flight speed and reflected the changes observed in the wake of the bats. In particular, several of the kinematic parameters reflected the differences in the function of the upstroke at low and high flight speeds. At lower flight speeds the bats use a pitch-up rotation to produce a backward flick which creates thrust and some weight support. At higher speeds this mechanism disappears and the upstroke generates weight support but no thrust. This is reflected by the changes in e.g. angle of attack, span ratio, camber and downstroke ratio. We also determined how different parameters vary throughout a wingbeat over the flight speeds studied. Both the camber and the angle of attack varied over the wingbeat differently at different speeds, suggesting active control of these parameters to adjust to the changing aerodynamic conditions. This study of the kinematics strongly indicates that the flight of bats is governed by an unsteady high-lift mechanism at low flight speeds and points to differences between birds and bats.

The near and far wake of Pallas' long tongued bat (Glossophaga soricina).

SUMMARY The wake structures of a bat in flight have a number of characteristics not associated with any of the bird species studied to this point. Unique features include discrete vortex rings generating negative lift at the end of the upstroke at medium and high speeds, each wing generating its own vortex loop, and a systematic variation in the circulation of the start and stop vortices along the wingspan, with increasing strength towards the wing tips. Here we analyse in further detail some previously published data from quantitative measurements of the wake behind a small bat species flying at speeds ranging from 1.5 to 7 m s–1 in a wind tunnel. The data are extended to include both near- and far-wake measurements. The near-/far-wake comparisons show that although the measured peak vorticity of the start and stop vortices decreases with increasing downstream distance from the wing, the total circulation remains approximately constant. As the wake evolves, the diffuse stop vortex shed at the inner wing forms a more concentrated vortex in the far wake. Taken together, the results show that studying the far wake, which has been the standard procedure, nevertheless risks missing details of the wake. Although study of the far wake alone can lead to the misinterpretation of the wake topology, the net, overall circulation of the main wake vortices can be preserved so that approximate momentum balance calculations are not unreasonable within the inevitably large experimental uncertainties.

Hierarchical strategy for relocating food targets in flower bats: spatial memory versus cue-directed search

The search and orientation behaviours used during foraging depend both on a foragers perceptual and memory abilities and on the spatiotemporal pattern of food distribution. We examined whether nectar-feeding bats using spatially and temporally predictable resources can pinpoint known flower targets within patches from a spatial memory-based approach alone or whether only a coarse-grained spatial memory requires local search for the targets object features within patches. We developed echoacoustically distinct geometric objects as unique acoustic ‘colour markers’ on experimental flowers. We could show that regional scale geometry of the local target environment influences orientation during target approach. Target choice was dependent on the relative positional information of local spatial cues when they were within a 20-cm radius around the target. For a dissociation experiment we first conditioned bats (in the laboratory and the Costa Rica rainforest) to a single target within an array of echoacoustically distinct feeders. During tests feeders were shifted and object cues rearranged. Bats directed initial choices most often at the feeder at the same absolute spatial coordinates as during the learning phase but later choices at the previously rewarded floral object cue. Thus bats had remembered both spatial and object attributes of their food target. However, their search strategy was to rely primarily on spatial memory and only secondarily on cue-based search. Flight approaches to feeders that were guided primarily by spatial memory were of significantly shorter duration than approaches that included active object-cue identification. This indicates a short-term energy advantage of the spatial memory-reliant strategy.

Compromised fidelity of endocytic synaptic vesicle protein sorting in the absence of stonin 2

Significance Brain function depends on neurotransmission, and alterations in this process are linked to neuropsychiatric disorders. Neurotransmitter release requires the rapid recycling of synaptic vesicles (SVs) by endocytosis. How synapses can rapidly regenerate SVs, yet preserve their molecular composition, is poorly understood. We demonstrate that mice lacking the endocytic protein stonin 2 (Stn2) show changes in exploratory behavior and defects in SV composition, whereas the speed at which SVs are regenerated is increased. As Stn2 is implicated in schizophrenia and autism in humans, our findings bear implications for neuropsychiatric disorders. Neurotransmission depends on the exocytic fusion of synaptic vesicles (SVs) and their subsequent reformation either by clathrin-mediated endocytosis or budding from bulk endosomes. How synapses are able to rapidly recycle SVs to maintain SV pool size, yet preserve their compositional identity, is poorly understood. We demonstrate that deletion of the endocytic adaptor stonin 2 (Stn2) in mice compromises the fidelity of SV protein sorting, whereas the apparent speed of SV retrieval is increased. Loss of Stn2 leads to selective missorting of synaptotagmin 1 to the neuronal surface, an elevated SV pool size, and accelerated SV protein endocytosis. The latter phenotype is mimicked by overexpression of endocytosis-defective variants of synaptotagmin 1. Increased speed of SV protein retrieval in the absence of Stn2 correlates with an up-regulation of SV reformation from bulk endosomes. Our results are consistent with a model whereby Stn2 is required to preserve SV protein composition but is dispensable for maintaining the speed of SV recycling.

OPERATIONAL TONGUE LENGTH IN PHYLLOSTOMID NECTAR-FEEDING BATS

Abstract Glossophagine bats (Phyllostomidae, Glossophaginae) are specialized visitors to the flowers of several hundred species of neotropical plants. They are able to exploit flowers in hovering flight by imbibing nectar with a highly protrusile brush-tip tongue. As tongue extension is achieved by muscular and vasohydraulic mechanisms, its operational length can be inferred only from actively feeding animals. For this study, we measured maximum tongue extensions during nectar feeding in 9 species of glossophagine bats. We trained bats to feed from vertically oriented glass test tubes (9- and 15-mm inside diameter). The maximum depth of nectar drainage by a bat was recorded as maximum operational tongue length. Measured operational tongue lengths were in the range of the total body length of bats. The record length was 77 mm (in tubes with 15-mm inside diameter) in the 17-g flower specialist Choeronycteris mexicana. This compares with only 11–24 mm in the nonglossophagine frugivorous bat Carollia perspicillata, an opportunistic nectar feeder. The capacity for tongue extension proves the specialized status of neotropical glossophagines as flower visitors and clearly distinguishes them anatomically and ecologically from nonglossophagine nectar-feeding bats.

Comparative aerodynamic performance of flapping flight in two bat species using time-resolved wake visualization.

Bats are unique among extant actively flying animals in having very flexible wings, controlled by multi-jointed fingers. This gives the potential for fine-tuned active control to optimize aerodynamic performance throughout the wingbeat and thus a more efficient flight. But how bat wing performance scales with size, morphology and ecology is not yet known. Here, we present time-resolved fluid wake data of two species of bats flying freely across a range of flight speeds using stereoscopic digital particle image velocimetry in a wind tunnel. From these data, we construct an average wake for each bat species and speed combination, which is used to estimate the flight forces throughout the wingbeat and resulting flight performance properties such as lift-to-drag ratio (L/D). The results show that the wake dynamics and flight performance of both bat species are similar, as was expected since both species operate at similar Reynolds numbers (Re) and Strouhal numbers (St). However, maximum L/D is achieved at a significant higher flight speed for the larger, highly mobile and migratory bat species than for the smaller non-migratory species. Although the flight performance of these bats may depend on a range of morphological and ecological factors, the differences in optimal flight speeds between the species could at least partly be explained by differences in their movement ecology.

Kinematics and wing shape across flight speed in the bat, Leptonycteris yerbabuenae

Summary The morphology and kinematics of a flying animal determines the resulting aerodynamic lift through the regulation of the speed of the air moving across the wing, the wing area and the lift coefficient. We studied the detailed three-dimensional wingbeat kinematics of the bat, Leptonycteris yerbabuenae, flying in a wind tunnel over a range of flight speeds (0–7 m/s), to determine how factors affecting the lift production vary across flight speed and within wingbeats. We found that the wing area, the angle of attack and the camber, which are determinants of the lift production, decreased with increasing speed. The camber is controlled by multiple mechanisms along the span, including the deflection of the leg relative to the body, the bending of the fifth digit, the deflection of the leading edge flap and the upward bending of the wing tip. All these measures vary throughout the wing beat suggesting active or aeroelastic control. The downstroke Strouhal number, Std, is kept relatively constant, suggesting that favorable flow characteristics are maintained during the downstroke, across the range of speeds studied. The Std is kept constant through changes in the stroke plane, from a strongly inclined stroke plane at low speeds to a more vertical stroke plane at high speeds. The mean angular velocity of the wing correlates with the aerodynamic performance and shows a minimum at the speed of maximum lift to drag ratio, suggesting a simple way to determine the optimal speed from kinematics alone. Taken together our results show the high degree of adjustments that the bats employ to fine tune the aerodynamics of the wings and the correlation between kinematics and aerodynamic performance.