Unusual echolocation behaviour of the common sword-nosed bat Lonchorhina aurita: an adaptation to aerial insectivory in a phyllostomid bat?

Most insectivorous bat species in the Neotropical family Phyllostomidae glean insects from ground, water or vegetation surfaces. They use similar and stereotypical echolocation calls that are generally very short (less than 1-3 ms), multi-harmonic and frequency-modulated (FM). By contrast, the common sword-nosed bat, Lonchorhina aurita, which has the longest noseleaf in the entire phyllostomid family, produces distinctly different echolocation calls. They are composed of a constant frequency (CF) component with a peak frequency of 45 kHz, followed by a short FM down-sweep at the end. With a mean call duration of 6.6 ms (max. 8.7 ms) when flying in the open they have the longest echolocation calls reported from phyllostomid bats. In cluttered environments, the CF-component is very short. In open habitats, however, L. aurita can emit pure CF-calls without the terminal FM-component. We also recorded in the field a distinct terminal group that closely resembles the feeding buzzes of aerial hawking bat species from other bat families. This is the first time the echolocation call design of L. aurita is presented. In addition, we contrast the echolocation behaviour of individuals flying in open and confined situations. Our results suggest that the unique echolocation system of L. aurita represents an adaptation to aerial hawking, a very unusual hunting mode within the phyllostomid family.

Finding flowers in the dark: nectar-feeding bats integrate olfaction and echolocation while foraging for nectar.

Nectar-feeding bats depend mainly on floral nectar to fulfil their energetic requirements. Chiropterophilous flowers generally present strong floral scents and provide conspicuous acoustic echoes to attract bats. While floral scents are assumed to attract bats over long distances, acoustic properties of flower structures may provide detailed information, thus supporting the localization of a flower at close ranges. So far, to our knowledge, there is no study trying to understand the relative importance as well as the combination of these generally coupled cues for detection (presence) and localization (exact position) of open flowers in nature. For a better comprehension of the significance of olfaction and echolocation in the foraging behaviour of nectar-feeding bats, we conducted two-choice experiments with Leptonycteris yerbabuenae. We tested the bats' behaviour in three experimental scenarios with different cues: (i) olfaction versus echolocation, (ii) echolocation versus echolocation and olfaction, and (iii) olfaction versus echolocation and olfaction. We used the floral scent of the bat-pollinated cactus Pachycereus pringlei as olfactory cue and an acrylic paraboloid as acoustic cue. Additionally, we recorded the echolocation behaviour of the bats and analysed the floral scent of P. pringlei. When decoupled cues were offered, bats displayed no preference in choice for any of the two cues. However, bats reacted first to and chose more often the coupled cues. All bats echolocated continuously and broadcast a long terminal group before a successful visit. The floral scent bouquet of P. pringlei is composed of 20 compounds, some of which (e.g. methyl benzoate) were already reported from chiropterophilous plants. Our investigation demonstrates for the first time to our knowledge, that nectar-feeding bats integrate over different sensory modes for detection and precise localization of open flowers. The combined information from olfactory and acoustic cues allows bats to forage more efficiently.

How Nectar-Feeding Bats Localize their Food: Echolocation Behavior of Leptonycteris yerbabuenae Approaching Cactus Flowers.

Nectar-feeding bats show morphological, physiological, and behavioral adaptations for feeding on nectar. How they find and localize flowers is still poorly understood. While scent cues alone allow no precise localization of a floral target, the spatial properties of flower echoes are very precise and could play a major role, particularly at close range. The aim of this study is to understand the role of echolocation for classification and localization of flowers. We compared the approach behavior of Leptonycteris yerbabuenae to flowers of a columnar cactus, Pachycereus pringlei, to that to an acrylic hollow hemisphere that is acoustically conspicuous to bats, but has different acoustic properties and, contrary to the cactus flower, present no scent. For recording the flight and echolocation behaviour we used two infrared video cameras under stroboscopic illumination synchronized with ultrasound recordings. During search flights all individuals identified both targets as a possible food source and initiated an approach flight; however, they visited only the cactus flower. In experiments with the acrylic hemisphere bats aborted the approach at ca. 40-50 cm. In the last instant before the flower visit the bats emitted a long terminal group of 10-20 calls. This is the first report of this behaviour for a nectar-feeding bat. Our findings suggest that L. yerbabuenae use echolocation for classification and localization of cactus flowers and that the echo-acoustic characteristics of the flower guide the bats directly to the flower opening.

Nectar uptake in bats using a pumping-tongue mechanism.

Many insects use nectar as their principal diet and have mouthparts specialized in nectarivory, whereas most nectar-feeding vertebrates are opportunistic users of floral resources and only a few species show distinct morphological specializations. Specialized nectar-feeding bats extract nectar from flowers using elongated tongues that correspond to two vastly different morphologies: Most species have tongues with hair-like papillae, whereas one group has almost hairless tongues that show distinct lateral grooves. Recent molecular data indicate a convergent evolution of groove- and hair-tongued bat clades into the nectar-feeding niche. Using high-speed video recordings on experimental feeders, we show distinctly divergent nectar-feeding behavior in clades. Grooved tongues are held in contact with nectar for the entire duration of visit as nectar is pumped into the mouths of hovering bats, whereas hairy tongues are used in conventional sinusoidal lapping movements. Bats with grooved tongues use a specific fluid uptake mechanism not known from any other mammal. Nectar rises in semiopen lateral grooves, probably driven by a combination of tongue deformation and capillary action. Extraction efficiency declined for both tongue types with a similar slope toward deeper nectar levels. Our results highlight a novel drinking mechanism in mammals and raise further questions on fluid mechanics and ecological niche partitioning.

Raman spectroscopy study of calcium oxalate extracted from cacti stems.

To find markers that distinguish the different Cactaceae species, by using near infrared Raman spectroscopy and scanning electron microscopy, we studied the occurrence, in the stem, of solid deposits in five Cactaceae species (Coryphantha clavata, Ferocactus latispinus, Opuntia ficus-indica, O. robusta, and O. strepthacantha) collected from their natural habitats from a region of México. The deposits in the tissues usually occurred as spheroidal aggregates, druses, or prismatic crystals. From the Raman spectra, the crystals were identified either as calcium oxalate monohydrate (CaC2O4·H2O) or calcium oxalate dihydrate (CaC2O4·2H2O). Opuntia species (subfamily Opuntioideae) showed the presence of CaC2O4·H2O, and the deposition of CaC2O4·2H2O was present in C. clavata and F. latispinus (subfamily Cactoideae, Cacteae tribe). As a punctual technique, Raman spectroscopy seems to be a useful tool to identify crystal composition. In addition to allowing the analysis of crystal morphology, this spectroscopic technique can be used to identify Cactaceae species and their chemotaxonomy.

Morphological specialization influences nectar extraction efficiency of sympatric nectar-feeding bats.

Mammals frequently use nectar as a supplementary food, while a predominantly nectarivorous lifestyle with morphological specializations for this feeding mode is rare within the class. However, Neotropical flower-visiting bats largely depend on nectar resources and show distinct adaptations to a nectar diet. Glossophagine bats form local guilds of 2-6 species that may differ distinctly in skull morphology. It is still unknown how and to what extent this morphological diversity influences the efficiency of nectar extraction and hence resource partitioning within the local bat guild. As foraging behaviour is a key factor for niche partitioning of co-existing species, we compared nectar extraction behaviour and efficiency at different flower depths among sympatric bat species with different degrees of morphological specialization (Glossophaga soricina, Leptonycteris yerbabuenae and Musonycteris harrisoni). In flight cage experiments with artificial flowers, at deeper nectar levels all species showed a distinct decrease in the amount of nectar extracted per visit and an increase in the time spent hovering at the flower, indicating increased energetic cost when foraging on longer tubed flowers. The lowest nectar extraction efficiency (g s(-1)) was found in the small G. soricina and the highest in the largest species L. yerbabuenae. However, when also considering the different energy requirements of the different-sized bat species, the morphologically most specialized M. harrisoni consistently showed the highest foraging efficiency. Our data suggest that the long rostrum and tongue of the extremely specialized M. harrisoni are probably not evolved for monopolization of co-evolved deep flowers but for allowing efficient access to the broadest range of the local chiropterophilous flower resources.