Adaptations to a diet of nectar and pollen in the marsupial Tarsipes rostratus (Marsupialia: Tarsipedidae)

The mouse-sized marsupial Tarsipes rostratus , endemic to south-western Australia, feeds almost exclusively on nectar and pollen. Its tongue has long filiform papillae at the tip and shorter compound papillae over much of the upper surface. These collect nectar and pollen when the long tongue, stiffened by a keratinized keel, is protruded into flowers or over pollen presenters. Pollen is scraped from the papillae by a series of combs on the roof of the mouth. A large diverticulum, off the main chamber of the stomach, may store nectar in times of surplus. Pollen is not digested in the stomach but during passage down the simple intestine, which does not have a caecum. In captive animals, pollen passed through the gut in about six hours and the percentage of grains voided which had lost their contents was related to time spent in the gut. The digestion process remains unresolved but probably takes place through the apertures in the shells of pollen grains. Tarsipes ingests large numbers of pollen grains whose contents probably provide necessary nutrients absent from nectar.     

Feeding by the short‐tailed bat (Mystacina tuberculata) on fruit and possibly nectar

New Zealand's short‐tailed bat (Mystacina tuberculata Gray, 1843) feeds on fruit, insects, and possibly nectar in North Island kauri (Agathis australis) forest. Fruits eaten by members of a colony of 500 bats in May included those of Freycinetia baueriana (Pandanaceae), Collospermum hastatum, and C. microspermum (Liliaceae). Pollen analyses of bat guano, and of the stomach contents of 4 short‐tailed bats from Omahuta Forest (Lat. 35°10'S) and 3 from Stewart Island and adjacent islands (Lat. 47°15'S), showed that most of the pollen was from flowers of Metrosideros and Leptospermum (Myrtaceae), Knightia excelsa (Proteaceae), and Collospermum, and that spores of the tree fern Cyathea (Cyatheaceae) were present also. Both Metrosideros and Knightia have abundant nectar. The partially extensile tongue of Mystacina is tipped with a brush of fine papillae, possibly to extract nectar and pollen; but the pollen and spores in the bat stomachs and guano could have come from insects eaten by the bats. Transverse ridges on the tongue may assist removal of juice from ripe fruits. These bats may disperse the small seeds of Freycinetia baueriana. The anatomical modifications of Mystacina for terrestrial and arboreal locomotion may have evolved primarily in response to its frugivorous and suspected nectarivorous habits.     

Seasonal reliance on nectar by an insectivorous bat revealed by stable isotopes

Many animals have seasonally plastic diets to take advantage of seasonally abundant plant resources, such as fruit or nectar. Switches from insectivorous diets that are protein rich to fruits or nectar that are carbohydrate rich present physiological challenges, but are routinely done by insectivorous songbirds during migration. In contrast, insectivorous bat species are not known to switch diets to consume fruit or nectar. Here, we use carbon stable isotope ratios to establish the first known case of a temperate bat species consuming substantial quantities of nectar during spring. We show that pallid bats (Antrozous pallidus) switch from a diet indistinguishable from that of sympatric insectivorous bat species in winter (when no cactus nectar is present) to a diet intermediate between those of insectivorous bats and nectarivorous bats during the spring bloom of a bat-adapted cactus species. Combined with previous results that established that pallid bats are effective pollinators of the cardon cactus (Pachycereus pringlei), our results suggest that the interaction between pallid bats and cardon cacti represents the first-known plant-pollinator mutualism between a plant and a temperate bat. Diet plasticity in pallid bats raises questions about the degree of physiological adaptations of insectivorous bats for incorporation of carbohydrate-rich foods, such as nectar or fruit, into the diet.     

Going to great lengths: selection for long corolla tubes in an extremely specialized bat–flower mutualism

In a hypothesis that has remained controversial since its inception, Darwin suggested that long-tubed flowers and long-tongued pollinators evolved together in a coevolutionary race, with each selecting for increasing length in the other. Although the selective pressures that flowers impose on tongue length are relatively straightforward, in that longer tongues allow access to more nectar, selective pressures that pollinators impose on flower length are less clear. Here, we test for such selective pressures in the highly specialized mutualism between the nectar bat Anoura fistulata, which can extend its tongue twice as far as other nectar bats, and Centropogon nigricans, which has flowers of a similar length (8–9 cm). We used flight cage experiments to examine the effects of artificially manipulated flower lengths on (i) bat behaviour and (ii) pollen transfer. Increased length produced longer visits, but did not affect the force bats applied during visits. In the second experiment, flower length increased both the male and female components of flower function: long male flowers delivered more pollen grains and long female flowers received more pollen grains. However, pollen transfer was not correlated with visit duration, so the mechanism behind differences in pollen transfer remains unclear. By demonstrating that bats select for increasing flower length, these results are consistent with the hypothesis that A. fistulata evolved its remarkable tongue in a coevolutionary race with long-tubed flowers similar to that envisioned by Darwin.     

A photographic account of pollen digestion by adult hoverflies

ABSTRACT. The method of pollen digestion by adults of the hoverfly Cheilosia albitarsis Mg. (Diptera: Syrphidae) was investigated by observing pollen grains at different stages in their progression along the gut. No form of mechanical 'grinding' to break up the grains was observed, as suggested by some previous authors. Instead, there was an exudation of the pollen grain contents through one of the pores in the pollen exine. This exudation may start as a growing pollen tube. The exact conditions which cause the pollen grains to give up their contents in this way are unknown, but it is suggested that nectar sugar within the gut may provide the necessary stimulus.     

Eucalyptus pollen grain emptying by two Australian nectarivorous psittacines

The relative importance of pollen as a source of protein to vertebrates is controversial. In nectarivorous psittacine birds, field studies support its importance, but an experimental study in a nectarivorous parrot showed that less than 7% of pollen grains were emptied. We investigated pollen grain emptying by two nectarivorous Australian parrots, the Swift Parrot Lathamus discolor and the Musk Lorikeet Glossopsitta concinna . We used a controlled experiment, and examined pollen located at different levels through the alimentary tract of wild L. discolor . There was significant emptying of pollen grains (x¯=45.4%±1.91 s.e.) by all birds in the experimental trials. There was also a progressive increase in the percentage of pollen grains emptied at different sites along the alimentary tract in wild birds (crop x¯=24.2%±4.44 s.e., proventriculus x¯=34.0%±7.29 s.e., duodenum x¯=54.3%±5.42 s.e. and distal intestine x¯=64.2%±4.68 s.e.). The percentage of pollen grains emptied by captive L. discolor in the experimental trial (x¯=44.1%±2.77 s.e.) was not significantly different from that found in wild L. discolor (x¯=40.3%±4.25 s.e.). Both species of nectarivorous parrot were able to rapidly ingest large quantities of Eucalyptus pollen and appeared to empty the pollen grains efficiently. Eucalyptus pollen appears to be an important source of protein for these birds.     

Nectar and Pollen Sources for Honeybee （Apis cerana cerana Fabr.） in Qinglan Mangrove Area, Hainan Island, China

In the present study, nectar and pollen sources for honeybee （Apls cerana cerana Fabr.） were studied in Qlnglan mangrove area, Hainan Island, China, based on microscopic analysis of honey and pollen load （corblcular and gut contents） from honeybees collected In October and November 2004. Qualitative and quantitative melittopalynologlcal analysis of the natural honey sample showed that the honey is of unlfloral type with Mimosa pudlca L. （Mlmosaceae） as the predominant （89.14%） source of nectar and pollen for A. cerana cerana In October. Members of Araceae are an Important minor （3%-15%） pollen type, whereas those of Arecaceae are a minor （〈3%） pollen type. Pollen grains of Nypa fruticans Wurmb., Rhlzophora spp., Excoecarla agallocha L., Lumnitzera spp., Brugulera spp., Kandella candel Druce, and Ceriops tagal （Perr.） C. B. Rob. are among the notable mangrove texa growing In Qinglan mangrove area recorded as minor taxa In the honey. The absolute pollen count （I.e. the number of pollen grains/10 g honey sample） suggests that the honey belongs to Group V （〉1 000 000）. Pollen analysis from the corblcular and gut contents of A. cerana cerana revealed the highest representation （95.60%） of members of Sonneratia spp. （Sonneratlaceae）, followed by Bruguiera spp. （Rhizophoraceae）, Euphorblaceae, Poaceae, Fabaceae, Arecaceae, Araceae, Anacardlaceae, and Rublaceae. Of these plants, those belonging to Sonneratla plants are the most Important nectar and pollen sources for A. cerana cerana and are frequently foraged and pollinated by these bees in November.     

Beyond the pollination syndrome: nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae)

Inga species present brush‐type flower morphology allowing them to be visited by distinct groups of pollinators. Nectar features in relation to the main pollinators have seldom been studied in this genus. To test the hypothesis of floral adaptation to both diurnal and nocturnal pollinators, we studied the pollination ecology of Inga sessilis, with emphasis on the nectar secretion patterns, effects of sequential removals on nectar production, sugar composition and the role of diurnal and nocturnal pollinators in its reproductive success. Inga sessilis is self‐incompatible and pollinated by hummingbirds, hawkmoths and bats. Fruit set under natural conditions is very low despite the fact that most stigmas receive polyads with sufficient pollen to fertilise all ovules in a flower. Nectar secretion starts in the bud stage and flowers continually secreting nectar for a period of 8 h. Flowers actively reabsorbed the nectar a few hours before senescence. Sugar production increased after nectar removal, especially when flowers were drained during the night. Nectar sugar composition changed over flower life span, from sucrose‐dominant (just after flower opening, when hummingbirds were the main visitors) to hexose‐rich (throughout the night, when bats and hawkmoths were the main visitors). Diurnal pollinators contributed less than nocturnal ones to fruit production, but the former were more constant and reliable visitors through time. Our results indicate I. sessilis has floral adaptations, beyond the morphology, that encompass both diurnal and nocturnal pollinator requirements, suggesting a complementary and mixed pollination system.     

Reproductive biology of Pachira aquatica Aubl. (Malvaceae: Bombacoideae): a tropical tree pollinated by bats,sphingid moths and honey bees

We investigated the reproductive biology, including the floral biology, pollination biology, breeding system and reproductive success, of Pachira aquatica, a native and dominant tropical tree of fresh water wetlands, throughout the coastal plain of the Gulf of Mexico. The flowers present nocturnal anthesis, copious nectar production and sugar concentration (range 18–23%) suitable for nocturnal visitors such as bats and sphingid moths. The main nocturnal visitors were bats and sphingid moths while bees were the main diurnal visitors. There were no differences in legitimate visitation rates among bats, moths and honey bees. Bats and honey bees fed mainly on pollen while moths fed on nectar, suggesting resource partitioning. Eight species of bats carried pollen but Leptonycteris yerbabuenae is probably the most effective pollinator due to its higher pollen loads. The sphingid moths Manduca rustica, Cocytius duponchel and Eumorpha satellitia were recorded visiting flowers. Hand pollination experiments indicated a predominant outcrossing breeding system. Open pollination experiments resulted in a null fruit set, indicating pollen limitation; however, mean reproductive success, according to a seasonal census, was 17 ± 3%; these contrasting results could be explained by the seasonal availability of pollinators. We conclude that P. aquatica is an outcrossing species with a pollination system originally specialized for bats and sphingid moths, which could be driven to a multimodal pollination system due to the introduction of honey bees to tropical America.     

Digestion of nectar and insects by Palestine sunbirds

In nectarivorous birds, specialization for feeding on nectar has led to a simple gut structure with high sugar digestive efficiencies and rapid gut passage rates. These features of the digestive system may make digestion of more complex, protein-rich food sources, such as pollen or insects, less efficient. In this light, we hypothesized that sugar metabolizability in nectarivorous Palestine sunbirds (Nectarinia osea) would be high, whereas nitrogen metabolizability would be lower than typically found for birds. We measured glucose and fructose apparent metabolizabilities (*MCs) and transit times (TTs) in eight Palestine sunbirds offered either a 10% or a 50% mixed sugar diet. *MC for glucose (99.9%+/-0.1%) was significantly greater than for fructose (99.6%+/-0.4%; ANOVA; P<0.001). TT for the 10% sugar diet (26.3+/-10.1 min) was significantly shorter than for the 50% sugar diet (47.0+/-7.8 min). We measured nitrogen true metabolizability (MC) and TT in Palestine sunbirds offered a daily fruit fly intake of either 40 or 200 flies. Nitrogen MC was not significantly different between diets, and average MC for both diets was 58.5%+/-8.5% (n=8). TT was not significantly different when birds ate 10 flies (50.1+/-13.6 min) than when they ate 50 flies (48.5+/-16.5 min). The high sugar *MC and relatively rapid TT of nectar in Palestine sunbirds are similar to those found for other nectarivorous species. Transit times of insect material are longer that those found in small insectivorous species. However, MCs of insect material are lower. Thus, even though sunbirds consume easily digestible soft-bodied insects, they are less efficient at extracting protein than nonnectarivores.     

Effects of habitat disruption on the activity of nectarivorous bats (Chiroptera: Phyllostomidae) in a dry tropical forest: implications for the reproductive success of the neotropical tree Ceiba grandiflora

In the tropical dry forest of the central Pacific coast of Mexico the pollination and reproductive success of the bombacaceous tree Ceiba grandiflora was negatively affected by habitat disruption. Two of the three bat species that function as effective pollinators for this species ( Glossophaga soricina and Musonycteris harrisoni) visited flowers found in trees in disturbed habitats significantly less than trees found in undisturbed habitats. A similar pattern was observed for the effective bat pollinator, Leptonycteris curasoae; however the difference was not significant. The three nectarivorous bats that functioned as effective pollinators of C. grandiflora also visited flowers to exclusively feed on pollen by biting or pulling off an anther (see Fig. S1 of Electronic Supplementary Material). The number of pollen grains deposited on stigmas from flowers in undisturbed areas was significantly greater than from flowers in disturbed habitats. The greater visitation rate and the greater number of pollen grains deposited on flowers from trees in undisturbed forest resulted in a significantly greater fruit set for trees in these areas. Our study demonstrates the negative effect that habitat disruption has on bat pollinators in tropical dry forest ecosystems and documents the negative consequences for the plants they pollinate.     

Cloning and Molecular Evolution of the Aldehyde Dehydrogenase 2 Gene (Aldh2) in Bats (Chiroptera)

Old World fruit bats (Pteropodidae) and New World fruit bats (Phyllostomidae) ingest significant quantities of ethanol while foraging. Mitochondrial aldehyde dehydrogenase (ALDH2, encoded by the Aldh2 gene) plays an important role in ethanol metabolism. To test whether the Aldh2 gene has undergone adaptive evolution in frugivorous and nectarivorous bats in relation to ethanol elimination, we sequenced part of the coding region of the gene (1,143 bp, ~73 % coverage) in 14 bat species, including three Old World fruit bats and two New World fruit bats. Our results showed that the Aldh2 coding sequences are highly conserved across all bat species we examined, and no evidence of positive selection was detected in the ancestral branches leading to Old World fruit bats and New World fruit bats. Further research is needed to determine whether other genes involved in ethanol metabolism have been the targets of positive selection in frugivorous and nectarivorous bats.     

Effectiveness of bats as pollinators of Stenocereus stellatus (Cactaceae) in wild, managed in situ, and cultivated populations in La Mixteca Baja, central Mexico

Stenocereus stellatus is an endemic, self-incompatible, columnar cactus found in central Mexico where many of its wild populations have been fragmented. As an economically important species of fruit-producing cactus, S. stellatus occurs in wild, managed in situ, and cultivated populations. The objectives of this study were to determine the effective pollinators of S. stellatus, to compare pollinator visits and reproductive parameters among the three types of populations, and to determine if nectar feeding-bats are moving among populations. Effective pollinators were the nectarivorous bats Choeronycteris mexicana, Leptonycteris curasoae, and L. nivalis. Fewer total visits per flower per night and fewer visits by Choeronycteris were observed in cultivated populations, while the opposite pattern was observed for Leptonycteris. One aggressive interaction was filmed in which Choeronycteris was physically displaced by Leptonycteris, and Choeronycteris visits were significantly affected by Leptonycteris visits. Cultivated populations received more pollen grains and had more fruit set. Variation in pollinator visits between different populations and the consequent effects on reproductive success were likely a result of competition between bat species, and differences in foraging and in sensitivity of bat species to human populations. Three marked L. curasoae traveled 15 km from their roosting site to their foraging area, and one visited cultivated and managed populations, suggesting that this species may be particularly important in moving pollen among populations.     

The potential significance of nectar‐feeding bats as pollinators in mangrove habitats of Peninsular Malaysia

We tested the hypothesis that bats are effective pollinators of mangroves in Malaysia. Bats (Eonycteris spelaea) visited flowers of two Sonneratia species frequently, and deposited large quantities of conspecific pollen grains on stigmas. The bats are likely to be important pollinators of the two mangrove species.     

Flight is the key to postprandial blood glucose balance in the fruit bats Eonycteris spelaea and Cynopterus sphinx

Excessive sugar consumption could lead to high blood glucose levels that are harmful to mammalian health and life. Despite consuming large amounts of sugar‐rich food, fruit bats have a longer lifespan, raising the question of how these bats overcome potential hyperglycemia. We investigated the change of blood glucose level in nectar‐feeding bats (Eonycteris spelaea) and fruit‐eating bats (Cynopterus sphinx) via adjusting their sugar intake and time of flight. We found that the maximum blood glucose level of C. sphinx was higher than 24 mmol/L that is considered to be pathological in other mammals. After C. sphinx bats spent approximately 75% of their time to fly, their blood glucose levels dropped markedly, and the blood glucose of E. spelaea fell to the fast levels after they spent 70% time of fly. Thus, the level of blood glucose elevated with the quantity of sugar intake but declined with the time of flight. Our results indicate that high‐intensive flight is a key regulator for blood glucose homeostasis during foraging. High‐intensive flight may confer benefits to the fruit bats in foraging success and behavioral interactions and increases the efficiency of pollen and seed disposal mediated by bats.     

Ammonia excretion increased and urea excretion decreased in urine of a new world nectarivorous bat with decreased nitrogen intake

We determined the effect of water and nitrogen intake on nitrogenous waste composition in the nectarivorous Pallas's long-tongued bat Glossophaga soricina (Phyllostomidae) to test the hypothesis that bats reduce excretion of urea nitrogen and increase the excretion of ammonia nitrogen as nitrogen intake decreases and water intake decreases. Because changes in urine nitrogen composition are expected only in animals whose natural diets are low in nitrogen and high in water content, we also measured maintenance nitrogen requirements (MNR). We hypothesized that, similar to other plant-eating vertebrates, nectarivorous bats have low MNR. Our nitrogen excretion hypothesis was partly proved correct. There was an increase in the proportion of N excreted as ammonia and a decrease in the proportion excreted as urea in low-nitrogen diets. The proportion of N excreted as ammonia and urea was independent of water intake. Most individuals were ureotelic (n = 28), and only a few were ureo-ammonotelic (n = 3) or ammonotelic (n = 2). According to our nitrogen requirement hypothesis, apparent MNR (60 mg kg(-0.75) d(-1)) and truly digestible MNR (54 mg N kg(-0.75) d(-1)) were low. A decrease in urea excretion in low-nitrogen diets may result from urea recycling from liver to the gut functioning as a nitrogen salvage system in nectarivorous bats. This mechanism probably contributes to the low MNR found in Pallas's long-tongued bats.     

Rat- and bat-pollination of Mucuna championii (Fabaceae) in Hong Kong

Mucuna (Fabaceae) species possess gullet-type flowers that open explosively and which are thought to be specifically adapted for bat- or bird-pollination. However, recent studies have shown that non-flying mammals are also important pollinators of this genus in Asia. Here we report on the pollination system of Mucuna championii (endemic in southeast China) in Hong Kong. As is typical for the genus, explosive opening is essential for fruit set, but flowers are unable to open in the absence of manipulation by an effective pollinator. Camera trap surveys of three individuals revealed both chestnut spiny rats (Niviventer fulvescens) and short-nosed fruit bats (Cynopterus sphinx) to be capable of triggering explosive opening. The number of flowers opened by each species did not differ significantly, and both removed most pollen grains from the flowers they visited, but either species visited different individuals. Sucrose-rich nectar was secreted by flowers throughout the day. Our results reveal that M. championii can be pollinated by both rats and bats, with this representing only the second report of rat-pollination in tropical Asia. The sympatric M. birdwoodiana often occurs in close proximity to M. championii and has an overlapping flowering season, suggesting that pollinator segregation may have played a role in shaping the evolutionary ecology of these two species.     

Impact of flowering on bird community dynamics in some central Victorian eucalypt forests

Many species of Eucalyptus in Australia provide copious amounts of nectar during their reproductive seasons. The nectar is used by many animal species but especially by birds, insects and some bats, which act as pollinators. One of the major features of eucalypt flowering in southern Australia is the patchy, asynchronous flowering of different species, which appears to drive mass nomadism of nectarivorous birds among regions and among habitats. Here we explore whether flowering asynchrony or climate is primarily responsible for the influxes and effluxes of vast numbers of nectarivorous birds in central Victoria, Australia. By using a structured sampling program, we show that winter flowering by red ironbark Eucalyptus tricarpa is the most likely agent controlling avian-nectarivore dynamics rather than climatic differences among regions. Densities and species richness of nectarivores, and numbers of nectarivory events, are all closely related to measures of flowering intensity. However, nonnectarivores, such as insectivores and granivores, show no relationships with either habitat or region. We discuss how dependence on a patchily distributed but highly rewarding resource such as nectar influences population densities and community structure in birds.     

Relationship between spatial working memory performance and diet specialization in two sympatric nectar bats

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.     

Pollen digestion by flower-feeding Scarabaeidae: protea beetles (Cetoniini) and monkey beetles (Hopliini)

Pollen protoplasm is very nutritious, but the hard and highly resistant outer wall (exine) of the pollen grain presents an obstacle that pollen-feeders must overcome to benefit from the valuable protoplasm. Pollen digestion in three pollen-eating scarab beetles, the green protea beetle Trichostetha fascicularis and two monkey beetle species, Peritrichia cinerea and Pachynema flavolineata, was investigated. Adult beetles were collected for observations of feeding mechanisms, scanning electron microscopy of mouthparts, and histological examination of gut contents. Serial sections of different regions along the gut were stained for different nutrients and examined to determine the appearance of the pollen grains and the removal of carbohydrates, proteins and lipids from the pollen. During feeding, beetles used dense brushes of setae on the tips of their maxillae to mop up nectar and sweep pollen into their mouths. Grains were ingested intact. Nutrients were effectively removed from the grains as they passed along the gut and most pollen grains in the hindgut were empty, with broken exines. All the beetles excreted the undigested exine. Comparison with other studies on pollen digestion by a variety of insect and vertebrate pollen-feeders suggests that digestive enzyme penetration of ingested pollen grains and exudation of the products of digestion is the most likely method used by these beetles.