Bats, flowers and fruit: evolutionary relationships in the Old World

Old World phytophagous bats (Megachiroptera: Pteropodidae) number 173 species of which 79% are Asian and 21% African. Bats arose, presumably monophyletically, in the early Tertiary, the Megachiroptera soon diverging from the Microchiroptera. By the Cretaceous-Tertiary boundary the major groups of modern angiosperms were present, some of these probably being pollinated nocturnally by large insects and non-flying mammals and others with seeds dispersed by terrestrial vertebrates. Early bats were perhaps initially attracted to such flowers and fruit by the insects found around them, later finding the plants themselves nutritious. Megabats today feed upon floral resources, fruit and leaves from a total of at least 188 plant genera in 64 families. They may effect both pollination and seed-dispersal, and both bat-flower and bat-fruit syndromes are commonly recognized. Individual species are generally catholic in their feeding, favoured food varying with locality and season. Depending upon roosting habits and season, megabats may travel considerable distances each night to feed and may undertake seasonal migrations. Their feeding in orchards may sometimes require their control, but the future of certain species is more seriously threatened by slaughter for food and particularly by habitat destruction.     

果蝠的婚配制度及繁殖策略

翼手类(Chiroptera)(俗称蝙蝠)分为小蝙蝠亚目(Microchiroptera)和大蝙蝠亚目(Megachiroptera),大蝙蝠又称果蝠或狐蝠,果蝠仅狐蝠科(Pteropodidae)1科188种。深入地了解其独特的婚配行为机制、独特的繁殖发育机制,对有效地开展果蝠的保护工作、合理地控制种群数量有积极意义。本文对果蝠的婚配制度及繁殖策略进行了阐述。     

Affording larger brains: testing hypotheses of mammalian brain evolution on bats

Several major hypotheses have been proposed to explain how larger brains in mammals, such as those of humans, are afforded in energetic terms. To date, these have been largely tested on primates, with some cross-mammal analysis. We use morphological, ecological, and metabolic data for 313 species of bats to examine the allometry of brain mass and to test key predictions from three of these hypotheses: the direct metabolic constraint, expensive tissue, and maternal energy hypotheses. We confirm that megachiropteran bats (entirely fruit-eating) have larger brains for their body mass than microchiropteran bats (fruit-eating and non-fruit-eating) and fruit-eating species (Megachiroptera and Microchiroptera) have larger brains than non-fruit-eating species (Microchiroptera). Although our analyses demonstrate little or no support for any of the three hypotheses, we show that 95.9% of the variance in brain mass can be explained by the independent effects of gestation length and body mass. This indicates that among bats, the duration of maternal investment plays an important role in the adult brain mass finally obtained. These analyses serve to emphasis the crucial importance of testing the general applicability of macroevolutionary hypotheses (often developed in isolation in one clade) in multiple clades with different evolutionary histories.     

Ecological observations on epomorphorine fruit-bats (Megachiroptera) in West African savanna woodland

Three species of Megachiroptera were studied in Mole National Park, Ghana, by systematic netting in various habitats and by observations of bats in the field and in captivity. This study, undertaken in July-August 1974 and 1975, is a preliminary attempt to elucidate how these species partition the resources available to them, with particular emphasis upon roosting habits, food resources, and temporal and spatial differences in foraging behaviour. All three species give birth towards the beginning of the wet season and are probably polyoestrus. The larger species, Epomophorus gambianus , does not appear to compete with the other two due to differences in roosting habits and the food resources available to it consequent upon its larger size. The two smaller species, Micropteropus pusillus and Nanonycteris veldkampi , are similar in size. N. veldkampi is presumed absent from Mole in the dry season when food is scarce; in the wet season it may minimise competition by being better adapted for nectarivory, foraging later, and foraging at a greater height than M. pusillus.     

Bats in bird nests in Australia: a review

Bats (Microchiroptera) utilize few types of bird nests as roosts. Ten species of bats (Molossidae and Vespertilionidae) were recorded roosting in the enclosed bottle-shaped mud nests of the Fairy Martin Hirundo ariel; two species (Vespertilionidae) were located in the hanging nests of scrubwrens Sericornis spp. and the Brown Gerygone Gerygone mouki; two species (Vespertilionidae) in the enclosed plant material nests of the Grey-crowned Babbler Pomatostomus temporalis and Fernwren Oreoscopus gutturalis; and one species (Emballonuridae) was recorded in the open cup-shaped nest of the White-rumped Swiftlet Collocalia spodiopygius. No information was available on the importance of bird nests as breeding sites and only one species, the Chocolate Wattled Bat Chalinolobus morio, has been recorded hibernating in a nest. Bird nests in Australia provide roosting habitat for four threatened bats and may be important to the conservation of these species.     

Molecular evolution inferred from immunological cross-reactivity of immunoglobulin G among Chiroptera and closely related species.

We examined the relationships between Megachiroptera and Microchiroptera, and between Chiroptera and other closely related species by the cross-reactivity of immunoglobulin epitopes. Rabbit polyclonal antibody to bat IgG was used for determining the cross-reactivity by a competitive ELISA method. Megachiroptera and Microchiroptera showed high cross-reactivity, over 95.3%, with each other. However, primates and insectivores showed very low cross-reactivity, 8.6 to 20.2% and 5.3 to 12.7%, respectively. These results suggest that suborders of Chiroptera are monophyletic and Chiroptera have a relatively closer relationship to primates than to insectivores.     

Comparative Roosting Ecology of Cynopterus (Chiroptera: Pteropodidae) Fruit Bats in Peninsular Malaysia1

Although the use of modified roosts has been reported in more than 20 species of bats in the tropics, comparative studies of the roosting ecology of congeneric tent‐roosting species are notably lacking. In the Paleotropics, this unique behavior has been described in two species belonging to the genus, Cynopterus: C. sphinx and C. brachyotis. However, it is not known whether tent roosting is an essential component of their roosting ecology, or whether the behavior is found in other members of the genus. In this study we characterize the roosting ecology of four sympatric species of Cynopterus in peninsular Malaysia and use these data to address two main questions. (1) Do all four species use modified roosts and, in those that do, is tent‐roosting obligate or opportunistic? (2) Do species pairs overlap in roost preferences and roosting habitat and, if so, is there evidence for interspecific interactions in relation to these resources? We radio‐tracked bats at two floristically distinct sites and located a total of 249 roosts. Interspecific roost niche overlap was minimal at both sites and we found no evidence for interspecific competition for roost resources at the local level. Species differences in roosting ecology were defined primarily by spatial separation of roosting habitats and secondarily by within‐habitat differences in roost selection. Importantly, we found that although periodic use of modified roosts was a characteristic shared by all four species, most roosts were unmodified, indicating that tent roosting is a facultative behavior in Malaysian Cynopterus.     

Biological correlates of extinction risk in bats

We investigated patterns and processes of extinction and threat in bats using a multivariate phylogenetic comparative approach. Of nearly 1,000 species worldwide, 239 are considered threatened by the International Union for Conservation of Nature and Natural Resources (IUCN) and 12 are extinct. Small geographic ranges and low wing aspect ratios are independently found to predict extinction risk in bats, which explains 48% of the total variance in IUCN assessments of threat. The pattern and correlates of extinction risk in the two bat suborders are significantly different. A higher proportion (4%) of megachiropteran species have gone extinct in the last 500 years than microchiropteran bats (0.3%), and a higher proportion is currently at risk of extinction (Megachiroptera: 34%; Microchiroptera: 22%). While correlates of microchiropteran extinction risk are the same as in the order as a whole, megachiropteran extinction is correlated more with reproductive rate and less with wing morphology. Bat extinction risk is not randomly distributed phylogenetically: closely related species have more similar levels of threat than would be expected if extinction risk were random. Given the unbalanced nature of the evolutionary diversification of bats, it is probable that the amount of phylogenetic diversity lost if currently threatened taxa disappear may be greater than in other clades with numerically more threatened species.     

Bat activity and species richness in different land‐use types in and around Chome Nature Forest Reserve,Tanzania

Bats have important ecological roles in ecosystems, but many species are threatened because of anthropogenic impacts. Tanzania has limited information on how bats respond to habitat modification. This makes it difficult to anticipate which bat species are at risk. Bat activity and species richness were assessed in five land‐use types: forest and banana–coffee (upland habitats), rice paddy, riverine and sisal estate (lowland habitats). Mist nets, harp traps and bat detectors were used to sample bats. Species richness differed between habitats. Bat activity levels were higher in lowland habitats than upland habitats. Riverine and rice paddy habitats were shown to have an important role as foraging sites for many insectivorous bats as bat species richness and activity were generally higher than other habitats. Fruit‐eating bats preferred riverine and banana–coffee habitats. We recommend using organic manure as alternatives to chemical fertilisers, and pesticide use should be avoided in rice paddies. Riparian vegetation along rivers and water bodies should be maintained as important faunal nesting, roosting and/or foraging grounds. The requirement that farming practices be at least 60 m from the river should be strictly enforced. These recommendations will help in the conservation of bats and their habitats in modified agricultural landscapes.     

A biological basis for bat conservation in British woodlands–a review

Fifteen species of insectivorous bats are resident in Britain. The numbers of most species have declined drastically in recent years and all are now fully protected under the Countryside and Wildlife Act 1981. Forests and woodlands offer foraging and roosting habitats for all species and it is important for Forest Managers to be aware of the impact which management practices may have on bat populations. Current knowledge on the importance of woodlands for roosting, feeding, water and breeding is reviewed and initial management guidelines for the enhancement of forests for bats proposed. Future research needs are discussed.     

Molecular evolution of bat color vision genes

The two suborders of bats, Megachiroptera (megabats) and Microchiroptera(microbats), use different sensory modalities for perceivingtheir environment. Megabats are crepuscular and rely on a well-developedeyes and visual pathway, whereas microbats occupy a nocturnalniche and use acoustic orientation or echolocation more thanvision as the major means of perceiving their environment. Inview of the differences associated with their sensory systems,we decided to investigate the function and evolution of colorvision (opsin genes) in these two suborders of bats. The middle/longwavelength (M/L) and short wavelength (S) opsin genes were sequencedfrom two frugivorous species of megabats, Haplonycteris fischeriand Pteropus dasymallus formosus, and one insectivorous speciesof microbat, Myotis velifer. Contrary to the situation in primates,where many nocturnal species have lost the functional S opsingene, both crepuscular and strictly nocturnal species of batsthat we examined have functional M/L and S opsin genes. Surprisingly,the S opsin in these bats may be sensitive to UV light, whichis relatively more abundant at dawn and at dusk. The M/L opsinin these bats appears to be the L type, which is sensitive tored and may be helpful for identifying fruits among leaves orfor other purposes. Most interestingly, H. fischeri has a recentduplication of the M/L opsin gene, representing to date theonly known case of opsin gene duplication in non-primate mammals.Some of these observations are unexpected and may provide insightsinto the effect of nocturnal life on the evolution of opsingenes in mammals and the evolution of the life history traitsof bats in general.     

Rainfall, food abundance and timing of parturition in African bats

We used published results from studies in Africa to test the hypothesis that the timing of parturition in the Chiroptera is constrained by rainfall. Comparison of year-round rainfall and insect data at various latitudes showed that insect abundance peaks approximately a month after peak rainfall. A similar comparison of parturition time to rainfall showed that with the possible exception of the molossids, the Microchiroptera commonly give birth a month before peak rainfall. With an average 6-week lactation period in the Microchiroptera, the timing of parturition is such that young bats are weaned just before the period of maximum insect abundance. We suggest that the needs of the young in this post-weaning period may be more important than the energetic demands of lactation on the mother in determining the timing of parturition on an evolutionary scale. A similar conclusion is implied for the African Megachiroptera, but there is insufficient information on their reproduction to adequately test the main hypothesis for these bats. Received: 4 October 1996 / Accepted: 14 March 1997     

The evolution of flight and echolocation in bats: another leap in the dark

The earliest known complete bats, from the Eocene (49–53 Mya), were already capable of flapping flight and echolocation. In the absence of direct fossil evidence there have been many speculative scenarios advanced to explain the evolution of these behaviours and their distributions in extant bats. Theories assuming chiropteran monophyly have generally presumed the ancestral pre‐bat was nocturnal, arboreal and insectivorous. Following this assumption hypotheses can be divided into the echolocation first, flight first and tandem development hypotheses, all of which assume that flight evolved only once in the lineage. In contrast, the chiropteran diphyly hypothesis suggests that flight evolved twice. Evidence supporting and refuting the different hypotheses are reviewed. It is concluded that there are significant problems attached to all the current models. A novel hypothesis is advanced, which starts from the assumption that bats are monophyletic and the ancestral pre‐bat was arboreal, but diurnal and frugivorous. After the evolution of flight it is suggested that these animals were driven into the nocturnal niche by the evolution of raptorial birds, and different groups evolved either specialised nocturnal vision (megachiropterans) or echolocation (microchiropterans). A block on sensory modality transfer has retained this distribution of perceptual capabilities ever since, despite some Megachiroptera evolving rudimentary echolocation, and the dietary convergence of some Microchiroptera with the Megachiroptera. The new hypothesis overcomes many of the problems identified in previous treatments.     

Can wing morphology inform conservation priorities for Southeast Asian cave bats?

Adaptations for foraging in the complex airspaces of forest interiors may make bat species in the Asian tropics particularly susceptible to forest loss. However, ecomorphological analysis of Vietnamese bat assemblages challenges the hypothesis that, due to their greater vagility, cave‐roosting bats are less vulnerable to habitat fragmentation than foliage‐roosting species. Of the 13 most highly adapted forest‐interior species in our study, eight were cave‐roosting members of the Rhinolophidae and Hipposideridae and had wing morphologies closely resembling five foliage‐roosting members of the Murininae and Kerivoulinae—species typically thought to have low vagility. Overall, both cave‐roosting and foliage‐roosting bats exhibited a wide range of flight indices and species' wing designs corresponded with preferred foraging habitats, suggesting that foraging strategy may outweigh roost preference as a determinant of bat wing morphology and flight performance. Consequently, where such variation occurs, cave‐roosting bat ensembles are likely to include species with low vagility and similar sensitivity to habitat fragmentation. This could have important conservation implications as Asian karst formations support high cave densities and important bat diversity yet increasingly represent forest refugia in anthropogenic landscapes. We, therefore, advocate greater consideration of species vagility in determining conservation priorities for the region's bat fauna.     

Novel paramyxoviruses in free-ranging European bats

The zoonotic potential of paramyxoviruses is particularly demonstrated by their broad host range like the highly pathogenic Hendra and Nipah viruses originating from bats. But while so far all bat-borne paramyxoviruses have been identified in fruit bats across Africa, Australia, South America, and Asia, we describe the detection and characterization of the first paramyxoviruses in free-ranging European bats. Moreover, we examined the possible impact of paramyxovirus infection on individual animals by comparing histo-pathological findings and virological results. Organs from deceased insectivorous bats of various species were sampled in Germany and tested for paramyxovirus RNA in parallel to a histo-pathological examination. Nucleic acids of three novel paramyxoviruses were detected, two viruses in phylogenetic relationship to the recently proposed genus Jeilongvirus and one closely related to the genus Rubulavirus. Two infected animals revealed subclinical pathological changes within their kidneys, suggestive of a similar pathogenesis as the one described in fruit bats experimentally infected with Hendra virus.Our findings indicate the presence of bat-born paramyxoviruses in geographic areas free of fruit bat species and therefore emphasize a possible virus-host co-evolution in European bats. Since these novel viruses are related to the very distinct genera Rubulavirus and Jeilongvirus, a similarly broad genetic diversity among paramyxoviruses in other Microchiroptera compared to Megachiroptera can be assumed. Given that the infected bats were either found in close proximity to heavily populated human habitation or areas of intensive agricultural use, a potential risk of the emergence of zoonotic paramyxoviruses in Europe needs to be considered.     

A mathematical model of the urine concentrating mechanism in the rat renal medulla. II. Functional implications of three-dimensional architecture

In a companion study [Layton AT. A mathematical model of the urine concentrating mechanism in the rat renal medulla. I. Formulation and base-case results. Am J Physiol Renal Physiol. (First published November 10, 2010). 10.1152/ajprenal.00203.2010] a region-based mathematical model was formulated for the urine concentrating mechanism in the renal medulla of the rat kidney. In the present study, we investigated model sensitivity to some of the fundamental structural assumptions. An unexpected finding is that the concentrating capability of this region-based model falls short of the capability of models that have radially homogeneous interstitial fluid at each level of only the inner medulla (IM) or of both the outer medulla and IM, but are otherwise analogous to the region-based model. Nonetheless, model results reveal the functional significance of several aspects of tubular segmentation and heterogeneity: 1) the exclusion of ascending thin limbs that reach into the deep IM from the collecting duct clusters in the upper IM promotes urea cycling within the IM; 2) the high urea permeability of the lower IM thin limb segments allows their tubular fluid urea content to equilibrate with the surrounding interstitium; 3) the aquaporin-1-null terminal descending limb segments prevent water entry and maintain the transepithelial NaCl concentration gradient; 4) a higher thick ascending limb Na(+) active transport rate in the inner stripe augments concentrating capability without a corresponding increase in energy expenditure for transport; 5) active Na(+) reabsorption from the collecting duct elevates its tubular fluid urea concentration. Model calculations predict that these aspects of tubular segmentation and heterogeneity promote effective urine concentrating functions.     

Emergence time in forest bats: the influence of canopy closure

The role of the forest canopy in protecting bats roosting in forest from predators is poorly known. We analysed the effect of canopy closure on emergence time in Barbastella barbastellus in a mountainous area of central Italy. We used radio-tracking to locate roosts and filmed evening emergence. Comparisons were made between roosts in open areas and those in dense forest. Median emergence time and illuminance were correlated. Moreover, from pregnancy to late lactation bats emerged progressively earlier, probably because of the exceptionally high wing loading affecting pregnant bats and the high energy demand of lactation. A significant influence of canopy closure on median emergence time was revealed after adjusting for the effects of light and reproductive state. Bats in open habitat emerged later than those roosting beneath closed canopy. In cluttered habitats, predators relying on vision may find it more difficult to detect and catch bats at light levels which would offer more chances of success when attacking prey in open habitats. Bats in dense forest are less vulnerable to predators and may take advantage of an earlier emergence by prolonging foraging. Although more vulnerable, lactating females roosting at open sites may benefit from warmer roosting conditions. Roosts in dense forest may be preferred under intense predation pressure. Forest management should favour canopy heterogeneity to provide bats with a range of roosting conditions. Our work emphasises the role of a fine-grained spatial scale in the roosting ecology of forest bats.     

Recent Transmission of a Novel Alphacoronavirus,Bat Coronavirus HKU10, from Leschenault's Rousettes to Pomona Leaf-Nosed Bats: First Evidence of Interspecies Transmission of Coronavirus between Bats of Different Suborders

Although coronaviruses are known to infect various animals by adapting to new hosts, interspecies transmission events are still poorly understood. During a surveillance study from 2005 to 2010, a novel alphacoronavirus, BatCoV HKU10, was detected in two very different bat species, Ro-BatCoV HKU10 in Leschenault''s rousettes (Rousettus leschenaulti) (fruit bats in the suborder Megachiroptera) in Guangdong and Hi-BatCoV HKU10 in Pomona leaf-nosed bats (Hipposideros pomona) (insectivorous bats in the suborder Microchiroptera) in Hong Kong. Although infected bats appeared to be healthy, Pomona leaf-nosed bats carrying Hi-BatCoV HKU10 had lower body weights than uninfected bats. To investigate possible interspecies transmission between the two bat species, the complete genomes of two Ro-BatCoV HKU10 and six Hi-BatCoV HKU10 strains were sequenced. Genome and phylogenetic analyses showed that Ro-BatCoV HKU10 and Hi-BatCoV HKU10 represented a novel alphacoronavirus species, sharing highly similar genomes except in the genes encoding spike proteins, which had only 60.5% amino acid identities. Evolution of the spike protein was also rapid in Hi-BatCoV HKU10 strains from 2005 to 2006 but stabilized thereafter. Molecular-clock analysis dated the most recent common ancestor of all BatCoV HKU10 strains to 1959 (highest posterior density regions at 95% [HPDs], 1886 to 2002) and that of Hi-BatCoV HKU10 to 1986 (HPDs, 1956 to 2004). The data suggested recent interspecies transmission from Leschenault''s rousettes to Pomona leaf-nosed bats in southern China. Notably, the rapid adaptive genetic change in BatCoV HKU10 spike protein by ∼40% amino acid divergence after recent interspecies transmission was even greater than the ∼20% amino acid divergence between spike proteins of severe acute respiratory syndrome-related Rhinolophus bat coronavirus (SARSr-CoV) in bats and civets. This study provided the first evidence for interspecies transmission of coronavirus between bats of different suborders.     

Within‐season changes in habitat use of forest‐dwelling boreal bats

Bats utilize forests as roosting sites and feeding areas. However, it has not been documented how bats utilize these habitats in the boreal zone with methods afforded by recent technological advances. Forest structure and management practices can create a variety of three‐dimensional habitats for organisms capable of flight, such as bats. Here, we study the presence of boreal bats in a forest forming a mosaic of different age classes, dominant tree species, canopy cover, soil fertility, and other environmental variables, throughout their active season in the summer using passive ultrasound detectors. Our results indicate a preference for mature forest by Eptesicus nilssonii and a pooled set of Myotis bats. Both groups of bats also showed temporal changes in their habitat use regarding forest age. In June and July, both groups occurred more often in mature than young forests, but from August onwards, the difference in occurrence became less evident in Myotis and disappeared completely in E. nilssonii. In addition, E. nilssonii was more often present in forests with low canopy cover, and its occurrence shifted from coniferous forests to deciduous forests during the season. The results reflect the within‐season dynamics of bat communities and their ability to utilize different types of forest as environmental conditions change. Yet, the results most importantly emphasize the importance of mature forests to bat diversity and the need to conserve such environments in the boreal zone.