The power requirements (Glossophaginae: Phyllostomidae) in nectar-feeding bats for clinging to flowers

Nectar-feeding bats are the heaviest pollinators exploiting flowers in a hovering foraging mode. As hovering flight is considered to be energetically costly, clinging to flowers would be beneficial from an energetic perspective. I examined the rate of oxygen consumption and carbon dioxide release during clinging flower visitation in two 10-g Glossophaga soricina (Glossophinae: Phyllostomidae) to evaluate the potential energetic benefit of clinging versus hovering. In addition, I measured the duration of flower visits of free-ranging glossophagine bats to Markea neurantha (Solanaceae), a bat-pollinated plant that allows both hovering and clinging flower visitation. After 20 s of clinging to an artificial respiratory mask, the bats respiratory exchange ratio did not significantly deviate from 1, indicating the combustion of sugar. The average oxygen uptake rate equaled 1.39 ml min^–1 (±0.38 SD, STPD) and the carbon dioxide release rate equaled 1.33 ml min^–1 (±0.20 SD, STPD) for feeder visits longer than 20 s (n=79). Converting the oxygen uptake rate into power input yielded 0.49 W, less than a third of the power requirements for hovering for a 10-g bat. Free-ranging 10-g glossophagine bats exploited flowers of M. neurantha for, on average, 0.32 s ( ±0.14 SD, n=273) during hovering and for 0.39 s (±0.18 SD, n=152) during clinging visitations. A comparison between the power requirements of flower exploitation in differently sized bats indicates that clinging would benefit larger nectar-feeding bats to a greater extent than smaller species.Communicated by G. Heldmaier     

Energetic cost of hovering flight in nectar-feeding bats (Phyllostomidae: Glossophaginae) and its scaling in moths, birds and bats

Three groups of specialist nectar-feeders covering a continuous size range from insects, birds and bats have evolved the ability for hovering flight. Among birds and bats these groups generally comprise small species, suggesting a relationship between hovering ability and size. In this study we established the scaling relationship of hovering power with body mass for nectar-feeding glossophagine bats (Phyllostomidae). Employing both standard and fast-response respirometry, we determined rates of gas exchange in Hylonycteris underwoodi (7 g) and Choeronycteris mexicana (13–18 g) during hover-feeding flights at an artificial flower that served as a respirometric mask to estimate metabolic power input. The O₂ uptake rate (V˙ _o2) in ml g⁻¹ h⁻¹ (and derived power input) was 27.3 (1.12 W or 160 W kg⁻¹) in 7-g Hylonycteris and 27.3 (2.63 W or 160 W kg⁻¹) in 16.5-g Choeronycteris and thus consistent with measurements in 11.9-g Glossophagasoricina (158 W kg⁻¹, Winter 1998). V˙ _o2 at the onset of hovering was also used to estimate power during forward flight, because after a transition from level forward to hovering flight gas exchange rates initially still reflect forward flight rates. V˙ _o2 during short hovering events (<1.5 s) was 19.0 ml g⁻¹ h⁻¹ (1.8 W) in 16-g Choeronycteris, which was not significantly different from a previous, indirect estimate of the cost of level forward flight (2.1 W, Winter and von Helversen 1998). Our estimates suggest that power input during hovering flight P _h (W) increased with body mass M (kg) within 13–18-g Choeronycteris (n = 4) as P _h  = 3544 (±2057 SE) M ^{1.76 (±0.21 SE)} and between different glossophagine bat species (n = 3) as P _h  = 128 (±2.4 SE) M ^{0.95 (±0.034 SE)}. The slopes of three scaling functions for flight power (hovering, level forward flight at intermediate speed and submaximal flight power) indicate that: 1. The relationship between flight power to flight speed may change with body mass in the 6–30-g bats from a J- towards a U-shaped curve. 2. A metabolic constraint (hovering flight power equal maximal flight power) may influence the upper size limit of 30–35 g for this group of flower specialists. Mass-specific power input (W kg⁻¹) during hovering flight appeared constant with regard to body size (for the mass ranges considered), but differed significantly (P < 0.001) between groups. Group means were 393 W kg⁻¹ (sphingid moths), 261 W kg⁻¹ (hummingbirds) and 159 W kg⁻¹ (glossophagine bats). Thus, glossophagine bats expend the least metabolic power per unit of body mass supported during hovering flight. At a metabolic power input of 1.1 W a glossophagine bat can generate the lift forces necessary for balancing 7 g against gravitation, whereas a hummingbird can support 4 g and a sphingid moth only 3 g of body mass with the same amount of metabolic energy. These differences in power input were not fully explained by differences in induced power output estimated from Rankine-Froude momentum-jet theory. Accepted: 10 November 1998     

Digestibility of columnar cacti pollen grains in the glosophagine bats Glossophaga longirostris and Leptonycteris curasoae (Chiroptera: Phyllostomidae)

We examined the protoplasmic assimilation of columnar cacti pollen grains in two species of Venezuelan desert glosophagine bats, Glossophaga longirostris and Leptonycteris curasoae, by determining the amount of empty (digested) pollen grains found in their fecal samples. To determine the amount of empty pollen grains, the fecal samples were stained to differ between empty and full (non-digested) pollen grains. The number of empty and full pollen grains observed in the fecal samples were corrected using the amount of aborted pollens present (before anthesis) in flowers of the columnar cacti species (Subpilocereus repandus, Stenocereus griseus and Pilosocereus tillianus) used by bats as food in the study site; G. longirostris and L. curasoae digested 64.2% and 71.3% of all the pollens fed, respectively. These high values confirm the importance of pollen in the diet of these bats, given its high nitrogen level.     

Phylogenetics and biogeography of the broad-nosed bats, genus Platyrrhinus (Chiroptera: Phyllostomidae)

The Neotropical broad-nosed bats, genus Platyrrhinus, represent a well-defined monophyletic group of 14 recognized species. A recent study of morphological characters confirmed Platyrrhinus monophyly and species diagnosis, but offered little support to their intra-specific relationships. We conducted phylogenetic analyses of the genus, using dense taxonomic sampling in combination with four gene sequences representing both mitochondrial and nuclear DNA transmission systems. Our aim was to elucidate the phylogenetic structure among species, using the resulting 3341 bp of DNA. Maximum parsimony, maximum likelihood, and Bayesian inference analyses produced similar topologies that confirm the monophyly of the genus Platyrrhinus and strongly support many previously unrecognized groups. Paraphyly of Platyrrhinus helleri and the unclear position of P. brachycephalus in the clades were also apparent in the data. Our biogeographical analysis suggests a Brazilian Shield origin for Platyrrhinus, followed by subsequent radiations of lineages in the Amazon Basin and Andes. Secondary dispersal from Amazonian and Andean centers is responsible for the Platyrrhinus inhabiting the Guianan Shield and the Pacific lowlands and Central America, respectively.     

Population dynamics, reproduction, and diet of the lesser long-nosed bat (Leptonycteris curasoae) in Jalisco, Mexico: implications for conservation

We estimate fluctuations in population size and sex ratio, documentbreeding behavior and reproduction, and determine the diet of a population ofthe lesser long-nosed bat, Leptonycteris curasoae, in anisland cave in Chamela Bay, Jalisco, Mexico, with monthly sampling during anannual cycle (October 1999–October 2000). Based on the area of thecave's ceiling and wall covered with L. curasoae inrelation to the potential roost area without them, in 1999 the abundanceincreased from 80% in October to 100% in November and December. In 2000 thepopulation decreased to 80% in January, 50% in February, 30% in March, 20% inApril, 10% in May, 5% in June and July, and less than 1% in August. Thepopulation rapidly increased to 60% in September and to 80% in October.Throughout the year there were significantly more males than females; however,there was significant heterogeneity over months. In September–Novemberthere were more females, but in December–August there were more malespresent. The majority of pregnant and lactating females were observed fromDecember to March and in July, while males were reproductive fromSeptember–January and in May–June. Breeding activity was observed inthe cave in November–December. Twenty-six species of plants were consumedduring the year, based on pollen identification from fecal samples. Bombacaceousspecies were the most important component of the diet from January to May andCactaceae were most important in June–September. Peak abundance and reproductive activitycoincided with peak flower resource availability, which occurred between Octoberand January and in June–July. The year-round presence and reproductiveactivity of L. curasoae at this site throughout the yeardemonstrate that many individuals are annual residents in this area and indicatethe importance of this roosting site. In order to develop a successfulconservation program for L. curasoae, in addition toprotecting migratory corridors and northern maternity roosts, it is equallyimportant to identify and protect areas that function as breeding colonies andyear-round sanctuaries for resident populations in the south.     

Seasonal distribution of the long-nosed bat (Leptonycteris curasoae) in North America: does a generalized migration pattern really exist?

Aim This paper examines the migration of the tropical nectarivorous bat Leptonycteris curasoae considered as a latitudinal migrant that breeds in south-west United States and northern Mexico in spring and migrates southward during fall. We tested the hypothesis that the latitudinal migration occurs only locally given by the local availability of bat resources, leading to migratory movements in zones with seasonal scarcity of resources and to resident bat populations where resources are available throughout the year. Localization We analysed the presence of L. curasoae along its distribution range in North America (between 14°N and 33°N). Study cases were also conducted in three Mexican localities: the Tehuacán Valley (17°48′–18°58′N and 96°48′–97°43′W), Sonoran Desert (28°41′N and 110°15′W), and the coast of Jalisco (19°32′N and 105°07′W). Methods Geographic evidence for latitudinal migration of L. curasoae was analysed using 94-year capture records housed in twenty-two collections of North America. Records were analysed using a Geographical Information System (GIS), in which floral resources and capture records were integrated. Monthly captures in the Tehuacán Valley were conducted during three years and bats abundance and reproductive status were correlated with the phenology of bat resources. Bat captures were also conducted during two consecutive years in an extratropical desert during winter and spring, and during one spring in the coast of Jalisco. Results The latitudinal migration of L. curasoae in North America only occurs at latitudes near 30°N, whereas bats may be residents at latitudes lower than 21°N. Captures were associated always to the availability of floral resources in both geographical and local scales. Main conclusions The existence of resident populations in the tropics with two reproductive events support the hypothesis that migration only occurs in the northern distribution limit of this nectar-feeding bat.     

Colour vision variation in leaf‐nosed bats (Phyllostomidae): Links to cave roosting and dietary specialization

Bats are a diverse radiation of mammals of enduring interest for understanding the evolution of sensory specialization. Colour vision variation among species has previously been linked to roosting preferences and echolocation form in the suborder Yinpterochiroptera, yet questions remain about the roles of diet and habitat in shaping bat visual ecology. We sequenced OPN1SW and OPN1LW opsin genes for 20 species of leaf‐nosed bats (family Phyllostomidae; suborder Yangochiroptera) with diverse roosting and dietary ecologies, along with one vespertilionid species (Myotis lavali). OPN1LW genes appear intact for all species, and predicted spectral tuning of long‐wavelength opsins varied among lineages. OPN1SW genes appear intact and under purifying selection for Myotis lavali and most phyllostomid bats, with two exceptions: (a) We found evidence of ancient OPN1SW pseudogenization in the vampire bat lineage, and loss‐of‐function mutations in all three species of extant vampire bats; (b) we additionally found a recent, independently derived OPN1SW pseudogene in Lonchophylla mordax, a cave‐roosting species. These mutations in leaf‐nosed bats are independent of the OPN1SW pseudogenization events previously reported in Yinpterochiropterans. Therefore, the evolution of monochromacy (complete colour blindness) has occurred in both suborders of bats and under various evolutionary drivers; we find independent support for the hypothesis that obligate cave roosting drives colour vision loss. We additionally suggest that haematophagous dietary specialization and corresponding selection on nonvisual senses led to loss of colour vision through evolutionary sensory trade‐off. Our results underscore the evolutionary plasticity of opsins among nocturnal mammals.     

Species diversity of bats (Mammalia: Chiroptera) in Iwokrama Forest, Guyana, and the Guianan subregion: implications for conservation

Fourteen species of bats are reported for the first time from Guyana (Saccopteryx gymnura, Micronycteris brachyotis, M. homezi, Lichonycteris obscura, Anoura latidens, Vampyressa pusilla, Vampyrodes caraccioli, Eptesicus chiriquinus, Cynomops paranus, Molossops neglectus, Molossus sp., Molossus coibensis, Molossus sinaloae, and Promops centralis) bringing the known bat diversity for the country to 121 species. Information including measurements, reproductive data, distribution, and taxonomy are provided for these species. Seven of these new records were collected in the Iwokrama International Rain Forest Programme site in central Guyana. Eighty-six bat species are now documented from Iwokrama Forest which is the highest species diversity for bats reported from any protected area in the world. There are, however, few tropical sites that have relatively complete inventories. A summary for bat species diversity in southern Venezuela, Guyana, Suriname, and French Guiana indicates that at least 146 species of bats are known from the Guianan subregion. Intense inventory surveys, especially in the often neglected subcanopy, suggest that species richness is probably underestimated in most Neotropical areas. Likewise, species-level diversity in the Guianan subregion is higher than previously suggested. Surveying and monitoring biodiversity are critical to developing a National Protected Areas System in Guyana.     

Reproduction of the Bat Glossophaga commissarisi (Phyllostomidae: Glossophaginae) in the Costa Rican Rain Forest During Frugivorous and Nectarivorous Periods1

I studied the reproduction of the 9 g nectarivorous bat Glossophaga commissarisi (Phyllostomidae: Glossophaginae) in relation to its food choice in a Costa Rican lowland rain forest over more than 2 yr. Reproduction was bimodal with birth peaks in April/May and October/November. The first birth peak coincided with a period of frugivory, whereas the second occurred during a period of almost exclusive nectarivory. All adult females recaptured in consecutive reproductive periods were reproductively active on both occasions, indicating that individual G. commissarisi females regularly reproduce twice per year at the study site. Throughout the annual cycle the mean testis length of the males correlated best with the proportion of females lactating, suggesting a post partum estrous pattern. Animals became reproductively active at about 1 yr of age. Fecal samples showed that females consumed significantly more insects than males.     

Foraging strategies,craniodental traits,and interaction in the bite force of Neotropical frugivorous bats (Phyllostomidae: Stenodermatinae)

1. Bats in the family Phyllostomidae exhibit great diversity in skull size and morphology that reflects the degree of resource division and ecological overlap in the group. In particular, the subfamily Stenodermatinae has high morphological diversification associated with cranial and mandibular traits that are associated with the ability to consume the full range of available fruits (soft and hard).
2. We analyzed craniodental traits and their relationship to the bite force in 343 specimens distributed in seven species of stenodermatine bats with two foraging strategies: nomadic and sedentary frugivory. We evaluated 19 traits related to feeding and bite force in live animals by correcting bite force with body size.
3. We used a generalized linear model (GLM) and post hoc tests to determine possible relationships and differences between cranial traits, species, and sex. We also used Blomberg''s K to measure the phylogenetic signal and phylogenetic generalized least‐squares (PGLS) to ensure the phylogenetic independence of the traits.
4. We found that smaller nomadic species, A. anderseni and A. phaeotis , have a similar bite force to the large species A. planirostris and A. lituratus; furthermore, P. helleri registered a bite force similar to that of the sedentary bat, S. giannae. Our study determined that all the features of the mandible and most of the traits of the skull have a low phylogenetic signal. Through the PGLS, we found that the diet and several cranial features (mandibular toothrow length, dentary length, braincase breadth, mastoid breadth, greatest length of skull, condylo‐incisive length, and condylo‐canine length) determined bite force performance among Stenodermatiane.
5. Our results reinforce that skull size is a determining factor in the bite force, but also emphasize the importance of its relationships with morphology, ecology, and phylogeny of the species, which gives us a better understanding of the evolutionary adaptions of this highly diverse Neotropical bat group.

     

Community of bat flies (Streblidae and Nycteribiidae) on bats in the Cerrado of Central-West Brazil: hosts,aggregation, prevalence,infestation intensity,and infracommunities

Streblidae and Nycteribiidae are families of bloodsucking flies that parasitize bats exclusively. We studied the community of these flies in a Cerrado area in the Central-West Brazil. We captured 708 bats over 17 nights from October 2012 to March 2013. Forty-five per cent of the hosts were parasitized by 836 specimens of bat flies of 22 species. The most abundant flies were Trichobius joblingi on Carollia perspicillata, followed by Megistopoda aranea on Artibeus planirostris, and Strebla guajiro on C. perspicillata. All bat flies showed a high level of specificity for their hosts. Trichobius joblingi was the bat fly with the highest prevalence (80%) and mean intensity of infestation (3.5) on hosts with a representative sample size (n > 20). This result is likely related to the type of roosting (cavity) used by C. perspicillata, primary host of this fly species. Anoura caudifer hosted the largest infracommunities (n = 7). However, most bats were parasitized by a single fly species, suggesting a pattern in infestations. The aggregation index was high, indicating an unequal occurrence in parasite infestations. The majority of hosts were infested by few or no flies and few hosts were highly infested, showing a negative binomial distribution.     

Anatomy and ultrastructure of the salivary (prosomal) glands in unfed water mite larvae Piona carnea (C.L. Koch, 1836) (Acariformes: Pionidae)

Anatomy and ultrastructure of prosomal salivary glands in the unfed water mite larvae Piona carnea (C.L. Koch, 1836) were examined using serial semi-thin sections and transmission electron microscopy. Three pairs of alveolar salivary glands shown are termed lateral, ventro-lateral and medial in accordance with their spatial position. These glands belong to the podocephalic system and are situated on the common salivary duct from back to forth in the above mentioned sequence. The arrangement of the medial glands is unusual because they are situated one after another on the medial (axial) body line, therefore they are termed anterior and posterior medial glands. The secretory duct of the anterior medial gland mostly turns right, and the duct of the posterior gland turns left. The salivary glands are located in the body cavity partly inside the gnathosoma and in the idiosoma in front of the brain (synganglion). Each gland is represented by a single acinus (alveolus) and is composed of several cone shaped secretory cells arranged around the large central (intra-acinar) cavity with the secretory duct base. The cells of all glands are filled with secretory vesicles of different electron density. The remaining cell volume is occupied by elements of rough endoplasmic reticulum, and the membrane enveloping vesicles may have ribosomes on its external surface. Large nuclei provided with large nucleoli occupy the basal cell zones. The pronounced development of the prosomal salivary glands indicates their important role in extra-oral digestion of water mite larvae.     

Roost Structure,Modification, and Availability in the White‐throated Round‐eared Bat,Lophostoma silvicolum (Phyllostomidae) Living in Active Termite Nests1

We studied roost structure, modification, and availability in Lophostoma silvicolum (Phyllostomidae), an insectivorous gleaning bat, on Barro Colorado Island (BCI), Panamá. Collection of nest material beneath termitaria and infrared video filming indicated that males of L. silvicolum excavate and maintain cavities inside active termite nests. A binary logistic regression analysis showed that to be suitable as roosts, termite nests have to be larger than 30 cm in diameter and taller than 30 cm, well shaded, with few transecting branches, and freely accessible from below. Use of active termite nests as roosts may provide several benefits to L. silvicolum, including reduction of competition for roost sites with sympatric bat species, reduced parasite load and a suitable microclimate. A comparison of number of all termite nests in selected forest plots with number of termite nests that are potentially suited as bat roosts and number of termite nests that are actually used by bats suggests that L. silvicolum may not be roost‐limited on BCI in spite of its highly specialized roost choice.     

Seasonal variation in glycoconjugates of the pedal glandular system of the rayed Mediterranean limpet,Patella caerulea (Gastropoda: Patellidae)

Glycoconjugates secreted by the pedal system of the rayed limpet, Patella caerulea, were characterised in situ by histochemical and lectin-histochemical methods in individuals collected around the annual cycle, in November, March, and June. Stainings with periodic acid–Schiff (PAS), Alcian blue pH 2.5 (AB pH 2.5), Alcian blue pH 1.0 (AB pH 1.0), high-iron diamine–Alcian blue pH 2.5 and lectin binding assays with 9 lectins (Con A, WGA, succinylated-WGA, PNA, DBA, SBA, AAA, UEA-I, LTA) were performed. Four secreting cell types were observed in the sole, one in the peripheric region, and two in the sidewall. Glycoconjugate composition varied among cell types and also in one and the same cell type throughout the year. β-Elimination followed by PAS and AB pH 2.5 stainings indicated that most saccharidic chains were O-linked to the protein backbone. Secretion by sole and peripheric region was acidic, carboxylated and/or sulfated, whereas that of the sidewall was neutral. Glucosaminylated and 1,4-fucosylated residuals were predominant in the cell types along the year, 1,2-fucosylated residuals being observed only in the sidewall cells in June. Mannosylated and/or glycosylated residuals were observed in all cells mostly in November. Galactosylated/galactosaminylated residuals were present mostly in the sidewall cells and in the sole subepidermal mucocytes in June. Mannosylated and/or glycosylated residuals in November are probably linked to gonad maturation or to higher locomotion and foraging activity, whereas galactosaminylation in the sole cells and 1,2-fucosylation and glucosaminylation in the sidewall cells in June are linked to a prolonged stationary state, increasing water adsorption to counteract dehydration and/or to modulate microbial interactions.     

Morphology and chemical composition of metathoracic scent glands in Dolycoris baccarum (Linnaeus, 1758) (Heteroptera: Pentatomidae)

One of the general defining characters of the Heteroptera is the presence of metathoracic scent glands (MTG). Using scanning electron microscopy, the morphology of the MTG of Dolycoris baccarum (Linnaeus 1758) (Heteroptera: Pentatomidae) was studied. The MTG belong to the diastomian type. The two glandular pores located between the mesothoracic and metathoracic coxae are associated with 'mushroom-like' structures. The MTG are composed of a reservoir and a pair of lateral glands is connected to the reservoir by a duct. A groove-like structure extends downwards from the ostiole. While this structure is long and wide, its ostiole is oval. Extracts of the volatile fractions from male and female MTG secretions were analysed by capillary gas chromatography–mass spectrometry (GC-MS) and exhibited a typical pentatomid composition. Seventeen chemical compounds were detected in female secretions, whereas 13 chemical compounds were detected in the male secretions. Most chemical compounds were similar between the sexes but were different in their quantities. In this regard, the compounds identified were investigated and the biological functions of the glandular secretions were discussed. In the analyses of the MTG of females of D. baccarum , tridecane (50.97%) was a major odour component and (Z,Z)-4,16-octadecadien-1-ol acetate (0.02%) was a minor odour component. In males, tridecane (50.80%) was a major odour component and 1,2-benzenedicarboxylic acid (0.02%) was a minor odour component.