Relationship between spatial working memory performance and diet specialization in two sympatric nectar bats.
ABSTRACT: Behavioural ecologists increasingly recognise spatial memory as one the most influential cognitive traits involved in evolutionary processes. In particular, spatial working memory (SWM), i.e. the ability of animals to store temporarily useful information for current foraging tasks, determines the foraging efficiency of individuals. As a consequence, SWM also has the potential to influence competitive abilities and to affect patterns of sympatric occurrence among closely related species. The present study aims at comparing the efficiency of SWM between generalist (Glossophaga soricina) and specialist (Leptonycteris yerbabuenae) nectarivorous bats at flowering patches. The two species differ in diet--the generalist diet including seasonally fruits and insects with nectar and pollen while the specialist diet is dominated by nectar and pollen yearlong--and in some morphological traits--the specialist being heavier and with proportionally longer rostrum than the generalist. These bats are found sympatrically within part of their range in the Neotropics. We habituated captive individuals to feed on artificial flower patches and we used infrared video recordings to monitor their ability to remember and avoid the spatial location of flowers they emptied in previous visits in the course of 15-min foraging sequences. Experiments revealed that both species rely on SWM as their foraging success attained significantly greater values than random expectations. However, the nectar specialist L. yerbabuenae was significantly more efficient at extracting nectar (+28% in foraging success), and sustained longer foraging bouts (+27% in length of efficient foraging sequences) than the generalist G. soricina. These contrasting SWM performances are discussed in relation to diet specialization and other life history traits.
Project description:<h4>Background</h4>The New World leaf-nosed bats (Phyllostomids) exhibit a diverse spectrum of feeding habits and innovations in their nutrient acquisition and foraging mechanisms. However, the genomic signatures associated with their distinct diets are unknown.<h4>Results</h4>We conducted a genomic comparative analysis to study the evolutionary dynamics related to dietary diversification and specialization. We sequenced, assembled, and annotated the genomes of five Phyllostomid species: one insect feeder (Macrotus waterhousii), one fruit feeder (Artibeus jamaicensis), and three nectar feeders from the Glossophaginae subfamily (Leptonycteris yerbabuenae, Leptonycteris nivalis, and Musonycteris harrisoni), also including the previously sequenced vampire Desmodus rotundus. Our phylogenomic analysis based on 22,388 gene families displayed differences in expansion and contraction events across the Phyllostomid lineages. Independently of diet, genes relevant for feeding strategies and food intake experienced multiple expansions and signatures of positive selection. We also found adaptation signatures associated with specialized diets: the vampire exhibited traits associated with a blood diet (i.e., coagulation mechanisms), whereas the nectarivore clade shares a group of positively selected genes involved in sugar, lipid, and iron metabolism. Interestingly, in fruit-nectar-feeding Phyllostomid and Pteropodids bats, we detected positive selection in two genes: AACS and ALKBH7, which are crucial in sugar and fat metabolism. Moreover, in these two proteins we found parallel amino acid substitutions in conserved positions exclusive to the tribe Glossophagini and to Pteropodids.<h4>Conclusions</h4>Our findings illuminate the genomic and molecular shifts associated with the evolution of nectarivory and shed light on how nectar-feeding bats can avoid the adverse effects of diets with high glucose content.
Project description:Every evening, from late spring to mid-summer, tens of thousands of hungry lactating female lesser long-nosed bats (Leptonycteris yerbabuenae) emerge from their roost and navigate over the Sonoran Desert, seeking for nectar and pollen [1, 2]. The bats roost in a huge maternal colony that is far from the foraging grounds but allows their pups to thermoregulate  while the mothers are foraging. Thus, the mothers have to fly tens of kilometers to the foraging sites-fields with thousands of Saguaro cacti [4, 5]. Once at the field, they must compete with many other bats over the same flowering cacti. Several solutions have been suggested for this classical foraging task of exploiting a resource composed of many renewable food sources whose locations are fixed. Some animals randomly visit the food sources , and some actively defend a restricted foraging territory [7-11] or use simple forms of learning, such as "win-stay lose-switch" strategy . Many species have been suggested to follow a trapline, that is, to revisit the food sources in a repeating ordered manner [13-22]. We thus hypothesized that lesser long-nosed bats would visit cacti in a sequenced manner. Using miniature GPS devices, aerial imaging, and video recordings, we tracked the full movement of the bats and all of their visits to their natural food sources. Based on real data and evolutionary simulations, we argue that the bats use a reinforcement learning strategy that requires minimal memory to create small, non-overlapping cacti-cores and exploit nectar efficiently, without social communication.
Project description: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 <i>Leptonycteris yerbabuenae</i>. 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 <i>Pachycereus pringlei</i> 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 <i>P. pringlei</i>. 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 <i>P. pringlei</i> 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.
Project description:Social insect foragers may specialize on certain resource types. Specialization on pollen or nectar among honeybee foragers is hypothesized to result from associations between reproductive physiology and sensory tuning that evolved in ancestral solitary bees (the Reproductive Ground-Plan Hypothesis; RGPH). However, the two non-honeybee species studied showed no association between specialization and ovary activation. Here we investigate the bumblebee B. impatiens because it has the most extensively studied pollen/nectar specialization of any bumblebee. We show that ovary size does not differ between pollen specialist, nectar specialist, and generalist foragers, contrary to the predictions of the RGPH. However, we also found mixed support for the second prediction of the RGPH, that sensory sensitivity, measured through proboscis extension response (PER), is greater among pollen foragers. We also found a correlation between foraging activity and ovary size, and foraging activity and relative nectar preference, but no correlation between ovary size and nectar preference. In one colony non-foragers had larger ovaries than foragers, supporting the reproductive conflict and work hypothesis, but in the other colony they did not.
Project description:Nectarivorous birds and bats have evolved highly specialized tongues to gather nectar from flowers. Here, we show that a nectar-feeding bat, Glossophaga soricina, uses dynamic erectile papillae to collect nectar. In G. soricina, the tip of the tongue is covered with long filamentous papillae and resembles a brush or mop. During nectar feeding, blood vessels within the tongue tip become engorged with blood and the papillae become erect. Tumescence and papilla erection persist throughout tongue retraction, and nectar, trapped between the rows of erect papillae, is carried into the mouth. The tongue tip does not increase in overall volume as it elongates, suggesting that muscle contraction against the tongue's fixed volume (i.e., a muscular hydrostat) is primarily responsible for tip elongation, whereas papilla erection is a hydraulic process driven by blood flow. The hydraulic system is embedded within the muscular hydrostat, and, thus, intrinsic muscle contraction may simultaneously increase the length of the tongue and displace blood into the tip. The tongue of G. soricina, together with the tongues of nectar-feeding bees and hummingbirds, which also have dynamic surfaces, could serve as valuable models for developing miniature surgical robots that are both protrusible and have highly dynamic surface configurations.
Project description: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.
Project description:Adaptation to pollinators is a key factor of diversification in angiosperms. The Caribbean sister genera Rhytidophyllum and Gesneria present an important diversification of floral characters. Most of their species can be divided in two major pollination syndromes. Large-open flowers with pale colours and great amount of nectar represent the generalist syndrome, while the hummingbird-specialist syndrome corresponds to red tubular flowers with a less important nectar volume. Repeated convergent evolution toward the generalist syndrome in this group suggests that such transitions rely on few genes of moderate to large effect. To test this hypothesis, we built a linkage map and performed a QTL detection for divergent pollination syndrome traits by crossing one specimen of the generalist species Rhytidophyllum auriculatum with one specimen of the hummingbird pollinated R. rupincola. Using geometric morphometrics and univariate traits measurements, we found that floral shape among the second-generation hybrids is correlated with morphological variation observed between generalist and hummingbird-specialist species at the genus level. The QTL analysis showed that colour and nectar volume variation between syndromes involve each one major QTL while floral shape has a more complex genetic basis and rely on few genes of moderate effect. Finally, we did not detect any genetic linkage between the QTLs underlying those traits. This genetic independence of traits could have facilitated evolution toward optimal syndromes.
Project description:Foraging specialization allows social insects to more efficiently exploit resources in their environment. Recent research on honeybees suggests that specialization on pollen or nectar among foragers is linked to reproductive physiology and sensory tuning (the Reproductive Ground-Plan Hypothesis; RGPH). However, our understanding of the underlying physiological relationships in non-<i>Apis</i> bees is still limited. Here we show that the bumblebee <i>Bombus terrestris</i> has specialist pollen and nectar foragers, and test whether foraging specialization in <i>B. terrestris</i> is linked to reproductive physiology, measured as ovarian activation. We show that neither ovary size, sensory sensitivity, measured through proboscis extension response (PER), or whole-body lipid stores differed between pollen foragers, nectar foragers, or generalist foragers. Body size also did not differ between any of these three forager groups. Non-foragers had significantly larger ovaries than foragers. This suggests that potentially reproductive individuals avoid foraging.
Project description:Nectar yeasts are common inhabitants of insect-pollinated flowers but factors determining their distribution are not well understood. We studied the influence of host identity, environmental factors related to pollution/urbanization, and the distance to a target beehive on local distribution of nectar yeasts within Robinia pseudoacacia L. and Tilia tomentosa Moench in Berlin, Germany. Nectar samples of six individuals per species were collected at seven sites in a 2?km radius from each target beehive and plated on YM-Agar to visualise the different morphotypes, which were then identified by sequencing a section of the 26S rDNA gene. Multivariate linear models were used to analyze the effects of all investigated factors on yeast occurrence per tree. Yeast distribution was mainly driven by host identity. The influence of the environmental factors (NO<sub>2</sub>, height of construction, soil sealing) strongly depended on the radius around the tree, similar to the distance of the sampled beehive. Incidence of specialist nectar-borne yeast species decreased with increasing pollution/urbanization index. Given that specialist yeast species gave way to generalist yeasts that have a reduced dependency on pollinators for between-flower dispersal, our results indicate that increased urbanization may restrict the movement of nectar-specialized yeasts, via limitations of pollinator foraging behavior.
Project description:Given their small size and high metabolism, nectar bats need to be able to quickly locate flowers during foraging bouts. Chiropterophilous plants depend on these bats for their reproduction, thus they also benefit if their flowers can be easily located, and we would expect that floral traits such as odor and shape have evolved to maximize detection by bats. However, relatively little is known about the importance of different floral cues during foraging bouts. In the present study, we undertook a set of flight cage experiments with two species of nectar bats (Anoura caudifer and A. geoffroyi) and artificial flowers to compare the importance of shape and scent cues in locating flowers. In a training phase, a bat was presented an artificial flower with a given shape and scent, whose position was constantly shifted to prevent reliance on spatial memory. In the experimental phase, two flowers were presented, one with the training-flower scent and one with the training-flower shape. For each experimental repetition, we recorded which flower was located first, and then shifted flower positions. Additionally, experiments were repeated in a simple environment, without background clutter, or a complex environment, with a background of leaves and branches. Results demonstrate that bats visit either flower indiscriminately with simple backgrounds, with no significant difference in terms of whether they visit the training-flower odor or training-flower shape first. However, in a complex background olfaction was the most important cue; scented flowers were consistently located first. This suggests that for well-exposed flowers, without obstruction from clutter, vision and/or echolocation are sufficient in locating them. In more complex backgrounds, nectar bats depend more heavily on olfaction during foraging bouts.