Bartonella spp. in Fruit Bats and Blood-Feeding Ectoparasites in Madagascar

We captured, ectoparasite-combed, and blood-sampled cave-roosting Madagascan fruit bats (Eidolon dupreanum) and tree-roosting Madagascan flying foxes (Pteropus rufus) in four single-species roosts within a sympatric geographic foraging range for these species in central Madagascar. We describe infection with novel Bartonella spp. in sampled Eidolon dupreanum and associated bat flies (Cyclopodia dubia), which nest close to or within major known Bartonella lineages; simultaneously, we report the absence of Bartonella spp. in Thaumapsylla sp. fleas collected from these same bats. This represents the first documented finding of Bartonella infection in these species of bat and bat fly, as well as a new geographic record for Thaumapsylla sp. We further relate the absence of both Bartonella spp. and ectoparasites in sympatrically sampled Pteropus rufus, thus suggestive of a potential role for bat flies in Bartonella spp. transmission. These findings shed light on transmission ecology of bat-borne Bartonella spp., recently demonstrated as a potentially zoonotic pathogen.     

Using Stable Isotopes to Infer the Impacts of Habitat Change on the Diets and Vertical Stratification of Frugivorous Bats in Madagascar

Human-modified habitats are expanding rapidly; many tropical countries have highly fragmented and degraded forests. Preserving biodiversity in these areas involves protecting species–like frugivorous bats–that are important to forest regeneration. Fruit bats provide critical ecosystem services including seed dispersal, but studies of how their diets are affected by habitat change have often been rather localized. This study used stable isotope analyses (δ¹⁵N and δ¹³C measurement) to examine how two fruit bat species in Madagascar, Pteropus rufus (n = 138) and Eidolon dupreanum (n = 52) are impacted by habitat change across a large spatial scale. Limited data for Rousettus madagascariensis are also presented. Our results indicated that the three species had broadly overlapping diets. Differences in diet were nonetheless detectable between P. rufus and E. dupreanum, and these diets shifted when they co-occurred, suggesting resource partitioning across habitats and vertical strata within the canopy to avoid competition. Changes in diet were correlated with a decrease in forest cover, though at a larger spatial scale in P. rufus than in E. dupreanum. These results suggest fruit bat species exhibit differing responses to habitat change, highlight the threats fruit bats face from habitat change, and clarify the spatial scales at which conservation efforts could be implemented.     

Hunting,disturbance and roost persistence of bats in caves at Ankarana,northern Madagascar

Surveys and monitoring of 37 caves in and around the Ankarana Special Reserve, northern Madagascar, yielded evidence of hunting of bats and potential disturbance of bats by miners and tourists, and colony counts for several bat species of potential conservation concern. Colony size decreased by 95% and 14% for a colony of Hipposideros commersoni and a colony of Eidolon dupreanum, respectively, when recent evidence of hunting occurred at those colonies and those declines are probably attributable to hunting. Evidence of hunting occurred commonly at the roosts of those species and most commonly at the roosts of Rousettus madagascariensis. Hunting of pteropodids was associated with high vulnerability of roosts to hunters, little forest buffer between the cave and open savannah and the absence of tombs in the cave. Roost sites of the hunted species persisted for at least several years and this regularity may facilitate hunting. This work supports the ranking of E. dupreanum, R. madagascariensis and H. commersoni as species of conservation concern. Managers should consider the impact of tourist visits on bats and of increasing access to caves for tourism. Conservation efforts for the hunted species should also seek to protect vulnerable and unprotected cave roosts.     

Searching for the Oldest Baobab of Madagascar: Radiocarbon Investigation of Large Adansonia rubrostipa Trees

We extended our research on the architecture, growth and age of trees belonging to the genus Adansonia, by starting to investigate large individuals of the most widespread Malagasy species. Our research also intends to identify the oldest baobabs of Madagascar. Here we present results of the radiocarbon investigation of the two most representative Adansonia rubrostipa (fony baobab) specimens, which are located in south-western Madagascar, in the Tsimanampetsotse National Park. We found that the fony baobab called “Grandmother” consists of 3 perfectly fused stems of different ages. The radiocarbon date of the oldest sample was found to be 1136 ± 16 BP. We estimated that the oldest part of this tree, which is mainly hollow, has an age close to 1,600 yr. This value is comparable to the age of the oldest Adansonia digitata (African baobab) specimens. By its age, the Grandmother is a major candidate for the oldest baobab of Madagascar. The second investigated specimen, called the “polygamous baobab”, consists of 6 partially fused stems of different ages. According to dating results, this fony baobab is 1,000 yr old. This research is the first investigation of the structure and age of Malagasy baobabs.     

Taking into account local practices and indigenous knowledge in an emergency conservation context in Madagascar

At the 5th World Parks Congress, held in Durban, South Africa in 2003, the President of Madagascar committed his government to tripling the country’s protected zones over the next 5 years. The announcement reflected a desire to combine rapid conservation efforts with sustainable development. Conservationists in Madagascar focused their attention on the endemic baobab tree, Adansonia grandidieri. This paper aims to identify the contradictions between the political emergency of the biodiversity conservation effort and local development needs. Eighty-three semi-structured interviews were conducted in two villages near the protected area of “Baobab Alley” in the Menabe region. Malagasy conservationists believed the area’s protected status would benefit the local economy through eco-tourism. However, the conservation actions undertaken there display limited understanding of local dynamics and conflict with farmers’ needs. To protect the baobabs, the government has prohibited rice cultivation without providing compensation. We show that the multifunctional baobab tree is integrated into an agroforestry system and protected by farmers. Based on these results, we address the issue of how to combine conservation and local development objectives through the involvement of farmers and the recognition of local knowledge in tree management. We also demonstrate that an emergency approach to conservation is not conducive to the successful integration of conservation and development.     

Habitat Use,Roost Selection and Conservation of Bats in Tsingy De Bemaraha National Park,Madagascar

Although the land mammals of Madagascar have been the subject of many studies, the island’s bats have yet to feature prominently on the research or conservation agenda. In this study we used mist nets, acoustic sampling and cave surveys to assess habitat use, seasonality and roost selection. Four microchiropteran species (Triaenops rufus, T. furculus, Miniopterus manavi and Myotis goudoti) appeared to be strongly associated with the forest interior based on trapping, but analysis of time-expanded echolocation recordings revealed that T. rufus and M.␣manavi were frequently recorded in forest edges and clearings. Bat activity was significantly lower inside the forest than at the interface between agricultural land and forest. The caves visited most often by tourists were low in bat abundance and species richness. Anjohikinakina Cave, which was visited infrequently by people, was used by five species and contained between 54% (winter) and 99% (summer) of bats counted in 16 caves and is a site of national importance for bat conservation. Hipposideros commersoni was only netted in our study area during October and may be a migrant to the site or present but inactive during the austral winter. The forest surrounding the caves is therefore important because it provides cover for emerging bats and a potential source of invertebrate prey whilst the forest edge is important to foraging bats.     

Human settlement and baobab distribution in south-western Mali

Aim Human settlement establishment and reproduction of the baobab tree (Adansonia digitata) appear spatially and temporally dependent because baobabs are abundant in many settlement sites in Africa. This paper tests the spatiotemporal relationship between baobab and settlement distribution. Location South‐western Mali. Methods In an area of 183 km², 1240 baobabs were located and mapped, their diameters measured, and habitat characteristics recorded for each individual. All occupied (n = 9) and abandoned (n = 84) settlements were located and mapped, and occupation dates were determined through interviews. Chi‐squared analysis indicated baobab habitat preferences, and bivariate point‐pattern analysis tested baobab–settlement spatiotemporal independence. Results Baobabs and human settlements are positively spatially associated at most distances and for all baobab size‐class–settlement age‐class pairs. However, positive spatial association is significant only at distances < 500 m, and young settlements and large baobabs are not significantly associated. Positive association between small and large baobabs is marginally significant at <300 m, but observed significance is less than that for baobab–settlement positive association. Baobab abundance is not evenly distributed across the range of habitats it occupies; recruitment is strongest in settlements and fields, and on cliffs, while mortality is highest on cliffs. Ethnographic observations suggest that human settlement practices and fruit use are the main human factors contributing to baobab–settlement positive spatial association. Main conclusions There are three main conclusions: (1) Human settlement and baobab recruitment are spatially dependant because settlement leads directly and indirectly to the development of baobab groves at settlement sites. (2) The lower than expected abundance of mature individuals in natural habitats, and the habitat preferences of the observed population, suggest that baobabs were introduced to south‐western Mali, probably centuries ago. (3) Human mobility over decadal time‐scales is necessary to maintain baobab population structure in landscapes dominated by shifting land use, where baobabs are not purposefully planted. Baobab population processes in such landscapes occur at the scale of human settlement.     

Bat Pollination Breakdown in the Caribbean Columnar Cactus Pilosocereus royenii1

Generalized pollination systems may be advantageous on island systems or regions of substantial disturbance. We examined whether or not specialization breakdown has occurred in a presumably bat‐pollinated columnar cactus, Pilosocereus royenii, on Puerto Rico, an island subjected to periodic hurricanes. The flowers show characteristics related to bat pollination including nocturnal anthesis, morphology, and amount and quality of nectar reward. The cactus produces flowers whose styles are temporally and mechanically separated from its anthers and do not self‐pollinate. Hand manipulations indicated that it is partially self‐incompatible or suffers some inbreeding depression. In 217 h of observations conducted biweekly over the course of 1 yr, P. royenii received visits from bats, moths, bees, and birds, but the only effective pollinator was the carpenter bee, Xylocopa mordax. Only four bat visits were recorded, all prior to stigma receptiveness. Floral morphology of P. royenii was significantly more variable than that of other bat‐pollinated species of the genus. We propose that infrequent bat visits are a consequence of a population crash and that floral variability is due to either relaxed selection for bat pollination or a transitional stage from bat pollination to bee pollination.     

Survey of Loxodonta africana (Elephantidae)‐caused bark injury on Adansonia digitata (Malavaceae) within Pendjari Biosphere Reserve,Benin

This study assessed the level of bark damage on baobab trees (Adansonia digitata) as caused by elephants (Loxodonta africana), and the possibility of finding refuges where baobab could escape bark damage within the Pendjari Biosphere Reserve (PBR). Distributions of elephants and baobab trees within the PBR were compared using presence records of both species taken along transect lines. Two sites (National Park vs. hunting zone) that differ in elephant density were compared for intensity of bark damage and correlations between the intensity of bark damage and stem size of the baobab trees and population structure of the baobab trees. Elephants and baobabs showed co‐occurrence in PBR suggesting that there is nowhere to hide for baobabs. The intensity of bark damage was positively correlated with elephant density and baobab girth. Baobab population girth classes were not significantly different in areas with and without bark damage. Future studies should test whether there are certain baobab genotypes that can resist elephant damage. It could also be tested whether effective conservation of elephants in the PBR has resulted in a bull‐biased population over its carrying capacity.     

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.     

Henipavirus RNA in African Bats

Background

Henipaviruses (Hendra and Nipah virus) are highly pathogenic members of the family Paramyxoviridae. Fruit-eating bats of the Pteropus genus have been suggested as their natural reservoir. Human Henipavirus infections have been reported in a region extending from Australia via Malaysia into Bangladesh, compatible with the geographic range of Pteropus. These bats do not occur in continental Africa, but a whole range of other fruit bats is encountered. One of the most abundant is Eidolon helvum, the African Straw-coloured fruit bat.

Methodology/Principal Findings

Feces from E. helvum roosting in an urban setting in Kumasi/Ghana were tested for Henipavirus RNA. Sequences of three novel viruses in phylogenetic relationship to known Henipaviruses were detected. Virus RNA concentrations in feces were low.

Conclusions/Significance

The finding of novel putative Henipaviruses outside Australia and Asia contributes a significant extension of the region of potential endemicity of one of the most pathogenic virus genera known in humans.     

Pollination system of the Pilosocereus leucocephalus columnar cactus (tribe Cereeae) in eastern Mexico

It has been suggested that there is a geographic dichotomy in the pollination systems of chiropterophilous columnar cacti: in intra‐tropical areas they are pollinated almost exclusively by bats, whereas in extratropical areas they are pollinated by bats, birds and bees. However, currently the studies are clumped both taxonomically (mainly Pachycereeae species) and geographically (mainly in the Tehuacan Valley and the Sonoran Desert). This clumping limits the possibility of generalising the pattern to other regions or cactus tribes. Only four of the 36 chiropterophilous cacti in Pilosocereus have been studied. Despite the tropical distribution of two Pilosocereus species, bees account for 40–100% of their fruit set. We examined how specialised is the pollination system of P. leucocephalus in eastern Mexico. As we studied tropical populations, we expected a bat‐specialised pollination system. However, previous studies of Pilosocereus suggest that a generalised pollination system is also possible. We found that this cactus is mainly bat‐pollinated (bats account for 33–65% of fruit set); although to a lesser degree, diurnal visitors also caused some fruit set (7–15%). Diurnal visitors were more effective in populations containing honeybee hives. P. leucocephalus is partially self‐compatible (14–18% of fructification) but unable to set fruit without visitors. Despite the variation in pollination system, P. leucocephalus shows more affinity with other columnar cacti from tropical regions than with those from extratropical regions. Although we report here that a new species of tropical Pilosocereus is relatively bat‐specialised, this Cereeae genus is more flexible in its pollination system than the Pachycereeae genera.     

Do artificial nectar feeders affect bat–plant interactions in an Ecuadorian cloud forest?

Plant–pollinator interactions are critical to ecosystems. However, when artificial nectar feeders are available in an area, they could draw pollinators away from plants. We tested the effects of artificial nectar feeders in an Ecuadorian cloud forest on four aspects of bat–plant interactions: (1) bat relative abundance; (2) bat pollen loads; (3) flower visitation rates, and (4) breeding success of a bat‐pollinated species (Burmeistera glabrata). We divided the study site into areas close to (~30 m) and far from (~500 m) three different feeder sites. At each distance, we captured nectar bats (Anoura caudifer, Anoura cultrata, and Lonchophylla robusta) to estimate their relative abundance and to collect pollen from fur and fecal samples. We also videotaped flowers to estimate bat visitation rates and recorded different breeding success variables of B. glabrata. We found that areas close to feeders have higher relative bat abundance by a factor of 40. In spite of this, the presence of feeders did not affect bat pollen loads, nor the flower visitation rates and breeding success of B. glabrata. Interestingly, there were differences in pollen loads between the three bat species, in that L. robusta individuals rarely carried pollen and were only captured near feeders.     

Analysis of Cathepsin and Furin Proteolytic Enzymes Involved in Viral Fusion Protein Activation in Cells of the Bat Reservoir Host

Bats of different species play a major role in the emergence and transmission of highly pathogenic viruses including Ebola virus, SARS-like coronavirus and the henipaviruses. These viruses require proteolytic activation of surface envelope glycoproteins needed for entry, and cellular cathepsins have been shown to be involved in proteolysis of glycoproteins from these distinct virus families. Very little is currently known about the available proteases in bats. To determine whether the utilization of cathepsins by bat-borne viruses is related to the nature of proteases in their natural hosts, we examined proteolytic processing of several viral fusion proteins in cells derived from two fruit bat species, Pteropus alecto and Rousettus aegyptiacus. Our work shows that fruit bat cells have homologs of cathepsin and furin proteases capable of cleaving and activating both the cathepsin-dependent Hendra virus F and the furin-dependent parainfluenza virus 5 F proteins. Sequence analysis comparing Pteropus alecto furin and cathepsin L to proteases from other mammalian species showed a high degree of conservation; however significant amino acid variation occurs at the C-terminus of Pteropus alecto furin. Further analysis of furin-like proteases from fruit bats revealed that these proteases are catalytically active and resemble other mammalian furins in their response to a potent furin inhibitor. However, kinetic analysis suggests that differences may exist in the cellular localization of furin between different species. Collectively, these results indicate that the unusual role of cathepsin proteases in the life cycle of bat-borne viruses is not due to the lack of active furin-like proteases in these natural reservoir species; however, differences may exist between furin proteases present in fruit bats compared to furins in other mammalian species, and these differences may impact protease usage for viral glycoprotein processing.     

Human activities link fruit bat presence to Ebola virus disease outbreaks

1. A significant link between forest loss and fragmentation and outbreaks of Ebola virus disease (EVD) in humans has been documented. Deforestation may alter the natural circulation of viruses and change the composition, abundance, behaviour and possibly viral exposure of reservoir species. This in turn might increase contact between infected animals and humans.
2. Fruit bats of the family Pteropodidae have been suspected as reservoirs of the Ebola virus. At present, the only evidence associating fruit bats with EVD is the presence of seropositive individuals in eight species and polymerase chain reaction-positive individuals in three of these.
3. Our study investigates whether human activities can increase African fruit bat geographical ranges and whether this influence overlaps geographically with EVD outbreaks that, in turn, are favoured by deforestation.
4. We use species observation records for the 20 fruit bat species found in favourable areas for the Ebola virus to determine factors affecting the bats' range inside the predicted Ebola virus area. We do this by employing a hypothetico-deductive approach based on favourability modelling.
5. We show that the range of some fruit bat species is linked to human activities within the favourable areas for the Ebola virus. More specifically, the areas where human activities favour the presence of five fruit bat species overlap with the areas where EVD outbreaks in humans were themselves favoured by deforestation. These five species are as follows: Eidolon helvum, Epomops franqueti, Megaloglossus woermanni, Micropteropus pusillus and Rousettus aegyptiacus. Of these five, all but Megaloglossus woermanni have recorded seropositive individuals. For the remaining 15 bat species, we found no biogeographical support for the hypothesis that positive human influence on fruit bats could be associated with EVD outbreaks in deforested areas within the tropical forest biome in West and Central Africa.
6. Our work is a useful first step allowing further investigation of the networks and pathways that may lead to an EVD outbreak. The modelling framework we employ here can be used for other emerging infectious diseases.

     

Characterization of 22 microsatellite marker loci in the Madagascar rousette (Rousettus madagascariensis)

Twenty-two nuclear microsatellite loci were isolated from a genomic DNA library derived from Madagascar’s Rousettus madagascariensis. Marker characteristics were determined from a single population (37 individuals) from Fort Dauphin (southeastern Madagascar). Sixteen of the 22 loci were within Hardy–Weinberg expectations. These loci are highly informative with polymorphic information content values ranging between 0.757 and 0.916. These loci will provide valuable information for the study of population genetics and gene flow within this species of bats. Due to the dramatic reduction and alteration of their habitat, data generated utilizing this marker suite will potentially provide additional information for the effective long-term management of this near-threatened bat species.     

Isolation of Salmonella Virchow from a Fruit Bat (Pteropus giganteus)

Detection of zoonotic pathogens carried by bats is important both for understanding disease ecology and for developing preventive measures. Pteropus fruit bats have been identified as potential carriers of Salmonella enterica serotype Typhi. A cross-sectional study was conducted to determine the prevalence of Salmonella Typhi and other Salmonella serotypes in Pteropus giganteus fruit bats in Bangladesh. Rectal swabs were collected from 302 bats and cultured for Salmonella species. The bats were trapped in three districts (Faridpur, Rajbari, and Cox’s Bazar). Salmonella Typhi was not found but one juvenile female bat from Faridpur district was positive for Salmonella Virchow. Close associations between frugivorous bats, humans, and livestock in rural Bangladesh make it likely that the bat was infected by consuming contaminated water.     

Ecological constraints on fruit initiation by Calyptrogyne ghiesbreghtiana (Arecaceae): FLORAL HERBIVORY,POLLEN AVAILABILITY,AND VISITATION BY POLLINATING BATS

Failure of a flower to initiate fruit can be attributed to an insufficiency of resources, genetic incompatibilities, or ecological constraints on pollination. Flower visitors can increase fruit initiation by pollinating flowers, or decrease fruit initiation by damaging them. If, however, resources limit fruit initiation, variation in visitation may be relatively unimportant. Visitors to Calyptrogyne ghiesbreghtiana, a rain forest understory palm, leave a record of their activity by feeding on floral tissue. I recorded variation in inflorescence visitation, floral display, and fruit initiation during 7 mo over two field seasons. On average, bats visited 50-60% of flowers; katydids and scarab beetles visited and damaged the remaining 40-50%. Four species of bat (Phyllostomidae) captured near inflorescences were found to be carrying C. ghiesbreghtiana pollen. Approximately 18% of flowers visited by bats and not damaged by insects initiated fruit, whereas insect-damaged flowers set a negligible number. Some variation in fruit initiation was explained by nightly variation in the proportion of inflorescences at each site that were potential pollen donors (male-phase inflorescences). Visitors responded to variation in floral display; katydids damaged more flowers on taller inflorescences, and in one season bats visited a greater proportion of flowers on inflorescences with many flowers. However, floral display only explained a small amount of variation in visitation. A similar amount of variation in flower visitation was explained by the degree to which inflorescences were obstructed by surrounding vegetation. I used path analysis to summarize the overall effect of floral display on visitation by both pollinators and florivores and the effect of visitation and site sex ratio on fruit initiation. Because almost all flowers were visited by bats or damaged by katydids, the amount of bat visitation was strongly negatively correlated with katydid damage. In spite of the low fruit set from bat-visited flowers, variation in bat visitation explained 27-37% of the variation in fruit initiation.     

Bat-pollinated Flower Assemblages and Bat Visitors at Two Atlantic Forest Sites in Brazil

A comparison between bat-pollinated plant assemblages at twosites in different altitudinal ranges covered by the Atlanticrainforest in southeastern Brazil is presented. The lowlands(5–90 m) harbour ten plant species in seven families,pollinated mostly by three glossophagine bat species. The highlands(1540–1600 m) harbour seven plant species in five families,pollinated by a single species of glossophagine. Bromeliadsaccount for about 30% of the bat-pollinated species at eachassemblage. Tube and brush shapes prevail in the flowers atboth sites. Corolla lengths averaged 26.8 and 37.2 mm, sugarconcentrations in nectar averaged 15.0 and 18.1%, and nectarvolumes averaged 150.8 and 167.0 µl in the lowland andhighland assemblages, respectively. The flowers are pollinatedmostly by glossophagine bats during hovering visits, and theplants are visited in the trap-line foraging pattern. The plantsbloom annually and both assemblages show a staggered continualflowering pattern. Flowering seasonality was found at both sites,with flowering clustering in the drier season at the lowlandsite and in the wetter season at the highland site. The ratiobetween bat-pollinated and hummingbird-pollinated species is0.24 at the lowland site and 0.23 at the highland one. Thesesimilar values indicate that additional studies on bat- andbird-pollinated assemblages are merited at other Atlantic rainforestsites.Copyright 1999 Annals of Botany Company Abutilon,bat-pollination,Dyssochroma, Eriotheca, Hillia, Lafoensia, Marcgravia,rainforest,Siphocampylus,southeastern Brazil,Tetrastylis, Vriesea.