Morphological and allozyme variation of Eidolon helvum (Mammalia: Megachiroptera) in the islands of the Gulf of Guinea

Morphological and genetic variation is evaluated among populations of the bat, Eidolon helvum , in the islands of the Gulf of Guinea (Central Africa). The populations from the islands of Bioko, Principe, and Sao Tome do not show significant phenetic differentiation, although a trend towards a reduction of size is found in the latter two islands. The low genetic distances between populations, as well as their values of Wright's fixation indexes, suggest that gene flow has hampered differentiation on these islands. In contrast, the population from Annobon, the smallest and farthermost island, shows remarkable morphological and genetic differentiation. On the mainland, E. helvum displays unique migratory and dispersal behaviours, but migratory behaviour was not found in any of the island populations. The combination of selective forces in harsher oceanic environments and restricted gene flow among populations appears to have favoured the high degree of morphological differentiation of E. helvum on Annobon. Due to the extended length of the dry season in Annobon, an earlier achievement of sexual maturity–and consequently smaller size—may be advantageous in the absence of migration. The differentiation is more marked among females, which also suggests that selection may be linked to the reproductive pattern. The population of the island of Annobon is herein described as a new subspecies, Eidolon helvum annobonensis subsp. nov.     

Comparative ecology of three pteropid bats in Rio Muni, West Africa

Data on morphologic features, habits, stratification, flight, and thermal response are presented for Eidolon helvum, Epomops franqueti , and Micropteropus pusillus from Rio Muni, West Africa. Relative abundance and reproduction activities of these pteropids are concordant with seasonal rainfall and availability of foods in Rio Muni. There are major differences between these sympatric species with regard to roosting sites, foods and feeding behaviour, levels of flight, and aerodynamic properties. Thermal responses vary between the species and are correlated with differences in behavioural thermoregulation.     

First application of satellite telemetry to track African straw-coloured fruit bat migration

Despite long-standing awareness of the potentially important ecological role of fruit bats, we know little about the ecology of the vast majority of species. Here we report the results of a pilot satellite tracking study aimed at establishing the scale of movement of the straw-coloured fruit bat Eidolon helvum . This was the first ever attempt to track African fruit bats using satellite telemetry. We tagged four bats with solar-charged 12 g satellite transmitters at Kasanka National Park in December 2005 and obtained a combined total of 104 different location fixes over a 149-day period. Before migrating, bats foraged as far as 59 km from the roost in a single evening; by contrast, one migrating individual moved 370 km in one night. Bats travelled an average 29 km day⁻¹ over the period of study, with bats that appeared to be migrating moving north-west from Kasanka at an average 90 km day⁻¹. The greatest cumulative distance travelled by a single bat was 2518 km in 149 days. The results show conclusively that the straw-coloured fruit bat E. helvum is capable of migrating thousands of kilometres across central Africa on an annual basis, implying that the fruit pulse in northern Zambia is richer than anything on offer in the Democratic Republic of the Congo at the same time of the year.     

Two novel parvoviruses in frugivorous New and Old World bats

Bats, a globally distributed group of mammals with high ecological importance, are increasingly recognized as natural reservoir hosts for viral agents of significance to human and animal health. In the present study, we evaluated pools of blood samples obtained from two phylogenetically distant bat families, in particular from flying foxes (Pteropodidae), Eidolon helvum in West Africa, and from two species of New World leaf-nosed fruit bats (Phyllostomidae), Artibeus jamaicensis and Artibeus lituratus in Central America. A sequence-independent virus discovery technique (VIDISCA) was used in combination with high throughput sequencing to detect two novel parvoviruses: a PARV4-like virus named Eh-BtPV-1 in Eidolon helvum from Ghana and the first member of a putative new genus in Artibeus jamaicensis from Panama (Aj-BtPV-1). Those viruses were circulating in the corresponding bat colony at rates of 7-8%. Aj-BtPV-1 was also found in Artibeus lituratus (5.5%). Both viruses were detected in the blood of infected animals at high concentrations: up to 10E8 and to 10E10 copies/ml for Aj-BtPV-1 and Eh-BtPV-1 respectively. Eh-BtPV-1 was additionally detected in all organs collected from bats (brain, lungs, liver, spleen, kidneys and intestine) and spleen and kidneys were identified as the most likely sites where viral replication takes place. Our study shows that bat parvoviruses share common ancestors with known parvoviruses of humans and livestock. We also provide evidence that a variety of Parvovirinae are able to cause active infection in bats and that they are widely distributed in these animals with different geographic origin, ecologies and climatic ranges.     

Roosting Requirements of Two Frugivorous Bats (Sturnira lilium and Arbiteus intermedius) in Fragmented Neotropical Forest1

As tropical forest fragmentation accelerates, scientists are concerned with the loss of species, particularly those that play important ecological roles. Because bats play a vital role as the primary seed dispersers in cleared areas, maintaining healthy bat populations is critical to natural forest regeneration. Observations of foraging bats suggest that many Neotropical fruit‐eating species have fairly general habitat requirements and can forage in many different kinds of disturbed vegetation; however, their roosting requirements may be quite different. To test whether or not general foraging requirements are matched by equally broad roosting requirements, we used radiotelemetry to locate roost sites of two common frugivorous bat species (Sturnira lilium and Artibeus intermedius) in a fragmented forest in southeastern Mexico. Sturnira lilium roosted inside tree cavities and selected large‐diameter roost trees in remnant patches of mature forest. Fewer than 2 percent of trees surveyed had a mean diameter equal to or greater than roost trees used by . S. lilium, Artibeus intermedius roosted externally on branches and vines and under palm leaves and selected roost trees of much smaller diameter. Compared to random trees, roost trees chosen by A. intermedius were closer to neighboring taller trees and also closer in height to these trees. Such trees likely provide cryptic roosts beneath multiple overlapping crowns, with sufficient shelter from predators and the elements. While males of A. intermedius generally roosted alone in small trees within secondary forest, females roosted in small groups in larger trees within mature forest and commuted more than three times farther than males to reach their roost sites. Loss of mature forest could impair the ability of frugivorous bats to locate suitable roost sites. This could have a negative impact on bat populations, which in turn could decrease forest regeneration in impacted areas.     

Ultrastructure of the ventricular myocardium of the bat Eidolon helvum

Ultrastructural studies, including a preliminary morphometric analysis, of the right ventricular myocardium in the West African bat Eidolon helvum show that the myocytes contain a wider T-tubule system and a higher proportion of mitochondria and lipid droplets than in typical terrestrial mammals such as the rat; these features in the bat are even mor pronounced than in hibernating species such as the golden hamster. In addition to having coupling arrangements with T-tubules and surface sarcolemma, cisterns of junctional sarcoplasmic reticulum are closely apposed to mitochondria and lipid droplets.     

Seasonal difference in the effects of fragmentation on seed dispersal by birds in Japanese temperate forests

Many studies have demonstrated that forest fragmentation reduces populations of animal species and causes local extinction, triggering many cascading effects. The effect of fragmentation on animals can be exerted through various processes, but such effects have been understudied. In this study, we posed the possibility of differences in the seasonal effects of fragmentation on frugivorous birds and their dispersal of seeds belonging to five tree species. We hypothesized that these effects may be caused by birds and their habitat selection for suitable breeding forests. We compared the abundance and species richness of frugivorous birds and the number of bird-removed fruits between a well-preserved and a fragmented temperate forest for two consecutive years. The abundance of birds was lower in the fragmented compared to the well-preserved forest during the breeding season, although no clear differences in species richness were observed. In contrast, similar decreases in bird abundance were not observed during the migratory season. After controlling for variation in crop size, the number of bird-removed fruits was lower in the fragmented forest compared to the well-preserved forest during the breeding season, but there was no such tendency during the migratory season. These results indicate that evaluations regarding the effects of fragmentation on seed dispersal that do not consider seasonal factors may lead to erroneous conclusions. This study suggests that the effects of fragmentation can be exerted though various processes, many of which remain poorly studied and warrant further examination.     

Process in the evolution of bird migration and pattern in avian ecogeography

Current ideas about the evolution of bird migration equate its origin with the first appearance of fully migratory populations, and attribute its evolution to a selective advantage generated by increased breeding success, gained through temporary emigration from resident populations to breed in under-exploited seasonal areas. I propose an alternative hypothesis in which migration first appears as a temporary directional shift away from the breeding site outside the reproductive period, in response to seasonal variation in the direction and/or severity of environmental gradients. Fully migratory populations then appear through either extinction of sedentary phenotypes, or colonisation of vacant seasonal areas by migrants. Where colonisation occurs, resident ancestral populations can be driven to extinction by competition from migrants which invade their range outside the breeding season, resulting in fully migratory species. An analogous process drives the evolution of migration between high latitudes and the tropics, since extension of breeding range into higher latitudes may drive low latitude populations to extinction, resulting in an overall shift of breeding range. This process can explain reverse latitudinal gradients in avian diversity in the temperate zone, since the breeding ranges of migratory species concentrate in latitudes where they enjoy the highest breeding success. Near absence of forest-dwelling species among Palaearctic-African migrants is attributable to the lack of forest in northern Africa for much of the Tertiary, which has precluded selection both for southward extension of migration by west Palaearctic forest species, and northward breeding colonisation by African forest species.     

Seeing the Forest through the Trees: Considering Roost-Site Selection at Multiple Spatial Scales

Conservation of bat species is one of the most daunting wildlife conservation challenges in North America, requiring detailed knowledge about their ecology to guide conservation efforts. Outside of the hibernating season, bats in temperate forest environments spend their diurnal time in day-roosts. In addition to simple shelter, summer roost availability is as critical as maternity sites and maintaining social group contact. To date, a major focus of bat conservation has concentrated on conserving individual roost sites, with comparatively less focus on the role that broader habitat conditions contribute towards roost-site selection. We evaluated roost-site selection by a northern population of federally-endangered Indiana bats (Myotis sodalis) at Fort Drum Military Installation in New York, USA at three different spatial scales: landscape, forest stand, and individual tree level. During 2007–2011, we radiotracked 33 Indiana bats (10 males, 23 females) and located 348 roosting events in 116 unique roost trees. At the landscape scale, bat roost-site selection was positively associated with northern mixed forest, increased slope, and greater distance from human development. At the stand scale, we observed subtle differences in roost site selection based on sex and season, but roost selection was generally positively associated with larger stands with a higher basal area, larger tree diameter, and a greater sugar maple (Acer saccharum) component. We observed no distinct trends of roosts being near high-quality foraging areas of water and forest edges. At the tree scale, roosts were typically in American elm (Ulmus americana) or sugar maple of large diameter (>30 cm) of moderate decay with loose bark. Collectively, our results highlight the importance of considering day roost needs simultaneously across multiple spatial scales. Size and decay class of individual roosts are key ecological attributes for the Indiana bat, however, larger-scale stand structural components that are products of past and current land use interacting with environmental aspects such as landform also are important factors influencing roost-tree selection patterns.     

Antibodies to henipavirus or henipa-like viruses in domestic pigs in Ghana, West Africa

Henipaviruses, Hendra virus (HeV) and Nipah virus (NiV), have Pteropid bats as their known natural reservoirs. Antibodies against henipaviruses have been found in Eidolon helvum, an old world fruit bat species, and henipavirus-like nucleic acid has been detected in faecal samples from E. helvum in Ghana. The initial outbreak of NiV in Malaysia led to over 265 human encephalitis cases, including 105 deaths, with infected pigs acting as amplifier hosts for NiV during the outbreak. We detected non-neutralizing antibodies against viruses of the genus Henipavirus in approximately 5% of pig sera (N = 97) tested in Ghana, but not in a small sample of other domestic species sampled under a E. helvum roost. Although we did not detect neutralizing antibody, our results suggest prior exposure of the Ghana pig population to henipavirus(es). Because a wide diversity of henipavirus-like nucleic acid sequences have been found in Ghanaian E. helvum, we hypothesise that these pigs might have been infected by henipavirus(es) sufficiently divergent enough from HeVor NiV to produce cross-reactive, but not cross-neutralizing antibodies to HeV or NiV.     

The breeding biology of equatorial vertebrates: reproduction in the fruit bat, Eidolon helvum, at latitude 0°20'N

The African fruit bat, Eidolon helvum Kerr, is known to occur only south of the Sahara where its distribution is localized. At 0°20' N, this bat exhibits seasonal and synchronized breeding the rhythm of which appears to correspond with the two rainfall peaks typical of Uganda. Quite unexpectedly and unprecedently, this bat exhibits delayed implantation lasting about three months. Evidence for this phenomenon comes from the histological examination of the adult female genital tracts which indicate that mating occurs only in April-June, but implanted embryos are only in evidence in October-November. The male sexual cycle corresponds to such a rhythm and shows a maximum testicular weight at the mating time. Births take place in February-March thus giving a gestation period of about four months. Only one young is born at a time and births occur just before the onset of the higher of the two rainfall peaks, presumably creating favourable conditions for the maximum survival of the young bats when weaned.     

Eating local: influences of habitat on the diet of little brown bats (Myotis lucifugus)

We employ molecular methods to profile the diet of the little brown bat, Myotis lucifugus, and describe spatial and temporal changes in diet over their maternity season. We identified 61 prey species of insects and 5 species of arachnid. The largest proportion of prey (～32%) were identified as species of the mass-emerging Ephemeroptera (mayfly) genus Caenis. Bats roosting in agricultural settings had lower dietary richness than those occupying a roost located on a forest fragment in a conservation area. We detected temporal fluctuations in diet over the maternity season. Dipteran (fly) species dominated the diet early in the season, replaced later by species of mayfly. Because our methodology provides species-level identification of prey, we were able to isolate environmental indicator species in the diet and draw conclusions about the location and type of their foraging habitat and the health of these aquatic systems. The species detected suggested that the bats use variable habitats; members of one agricultural roost foraged on insects originating in rivers or streams while those in another agricultural roost and the forest roost fed on insects from pond or lake environments. All source water for prey was of fair to good quality, though no species detected are intolerant of pollution thus the habitat cannot be classified as pristine. Our study outlines a model system to investigate the abiotic and biotic interactions between habitat factors through this simple food chain to the top predator.     

Bartonella species in bat flies (Diptera: Nycteribiidae) from western Africa

Bat flies are obligate ectoparasites of bats and it has been hypothesized that they may be involved in the transmission of Bartonella species between bats. A survey was conducted to identify whether Cyclopodia greefi greefi (Diptera: Nycteribiidae) collected from Ghana and 2 islands in the Gulf of Guinea harbour Bartonella. In total, 137 adult flies removed from Eidolon helvum, the straw-coloured fruit bat, were screened for the presence of Bartonella by culture and PCR analysis. Bartonella DNA was detected in 91 (66·4%) of the specimens examined and 1 strain of a Bartonella sp., initially identified in E. helvum blood from Kenya, was obtained from a bat fly collected in Ghana. This is the first study, to our knowledge, to report the identification and isolation of Bartonella in bat flies from western Africa.     

Scale-Dependent Effects of Landscape Structure and Composition on Diurnal Roost Selection by Forest Bats

Abstract: Forest management affects the quality and availability of roost sites for forest-dwelling bats, but information on roost selection beyond the scale of individual forest stands is limited. We evaluated effects of topography (elevation, slope, and proximity of roads and streams), forest habitat class, and landscape patch configuration on selection of summer diurnal roosts by 6 species of forest-dwelling bats in a diverse forested landscape of the Ouachita Mountains, Arkansas, USA. Our objectives were to identify landscape attributes that potentially affect roost placement, determine whether commonalities exist among species in their response to landscape attributes, and evaluate the effects of scale. We modeled roost selection at 2 spatial scales (250- and 1,000-m radius around each roost). For each species, parameters included in models differed between the 2 scales, and there were no shared parameters for 2 species. Average coefficients of determination (R²) for small-scale models were generally higher than for large-scale models. Abundance of certain forest habitat classes were included more often than patch configuration or topography in differentiating roost from random locations, regardless of scale, and most species were more likely to roost in areas containing abundant thinned forest. Among topographic metrics, big brown bats (Eptesicus fuscus) were more likely to roost at higher elevations; roosts of big brown bats, northern long-eared bats (Myotis septentrionalis), and Seminole bats (Lasiurus seminolus) were influenced by slope; and big brown bats, evening bats (Nycticeius humeralis), and Seminole bats were more likely to roost closer to water than random. Northern long-eared bats and red bats (Lasiurus borealis) were more likely to roost closer to roads, whereas eastern pipistrelles (Perimyotis subflavus) were more likely to roost further from roads than random. Common parameters in most models included 1) positive associations with group selection (5 of 6 species) and thinned mature forest (4 species) at the small scale; 2) negative associations with unmanaged mixed pine-hardwood forest 50–99 years old at the large scale (4 species); 3) negative association with stands of immature pine 15–29 years old at the small scale (3 species); and 4) a positive association with largest patch index at the large scale (3 species). Our results suggest that, in a completely forested landscape, a variety of stand types, seral stages, and management conditions, varying in size and topographic location throughout the landscape, would likely provide the landscape components for roosting required to maintain a diverse community of forest bats in the Ouachita Mountains.     

Drove roads: Keystone structures that promote ant diversity in Mediterranean forest landscapes

Drove roads are the traditional corridors used by pastoralists for seasonal movements of livestock (transhumance). They cover a considerable land area in Mediterranean countries and, although they are an obvious source of landscape diversity, their influence on the diversity and composition of animal assemblages has not been documented. Ant communities were studied on four active drove roads, two in forests (submediterranean and conifer) and two in open environments (croplands and rangelands). They were compared with the respective matrix communities and their contribution to local species richness was evaluated. The effects were heavily dependent on the open or closed nature of the matrix. In forest environments, drove roads increased ant species richness at the local scale, acting as clear keystone structures. Their species richness and functional diversity were highest on the fine scale, species composition was different, and a slight edge effect in the matrix was detected. In contrast, drove roads had little or even a negative effect in open environment locations. We conclude that drove roads have a high conservation value for ants in Mediterranean forest environments, in addition to their importance as reservoirs of plant biodiversity and generators of ecological goods and services.     

Roosting behavior of a Neotropical migrant songbird, the northern waterthrush Seiurus noveboracensis, during the non-breeding season

Several species of Nearctic-Neotropical migratory songbirds appear to form roosting aggregations while on their wintering grounds but little is understood about the ecology of this behavior. We studied roosting behavior and patterns of roost habitat selection in the northern waterthrush Seiurus noveboracensis , during three winter years (2002–2004) in Puerto Rico using radio telemetry. Overall, red mangrove was selected for roosting disproportionately to its availability. Regardless of diurnal habitat used, 87% (n=86) of northern waterthrush selected dense stands of coastal red mangrove for roost sites. Individuals traveled up to 2 km to access roost sites in this habitat on a daily basis. The majority (8 of 14) of individuals roosted alone, while others roosted in loose aggregations near communal roosts of gray kingbirds Tyrannus dominicensis . Patterns of roost site selection did not vary by sex. Individuals showing aggressive response to playback during the day, however, selected roost sites significantly closer to the coast. Several additional migratory and resident bird species also used red mangrove for night-time roosting habitat. Red mangrove may be a critical nocturnal roosting habitat for bird populations that live in proximity to coastal areas in the Neotropics. The benefits of nocturnal roosting behavior as well as why individuals appear to select red mangrove remain poorly understood.     

Determining fine‐scale migratory connectivity and habitat selection for a migratory songbird by using new GPS technology

Migratory aerial insectivores are among the fastest declining avian groups, but our understanding of these trends has been limited by poor knowledge of migratory connectivity and the identification of critical habitat across the vast distances they travel annually. Using new, archival GPS loggers, we tracked individual purple martins Progne subis from breeding colonies across North America to determine precise (< > 10 m) locations of migratory and overwintering roost locations in South America and to test hypotheses for fine‐scale migratory connectivity and habitat use. We discovered weak migratory connectivity at the roost scale, and extensive, fine‐scale mixing of birds in the Amazon from distant (> 2000 km) breeding sites, with some individuals sharing the same roosting trees. Despite vast tracts of contiguous forest in this region, birds occupied a much more limited habitat, with most (56%) roosts occurring on small habitat islands that were strongly associated with water. Only 17% of these roosts were in current protected areas. These data reflect a critical advance in our ability to remotely determine precise migratory connectivity and habitat selection across vast spatial scales, enhancing our understanding of population dynamics and enabling more effective conservation of species at risk.     

Demographic and spatial responses of resident bird populations to the arrival of migratory birds within an urban environment

Long-distance migration allows many bird species to overcome the severe climatic changes that occur in seasonal environments. Migration is highly demanding, and given its cyclical nature, we currently know that it has substantial effects on the population parameters of migratory birds during both breeding and wintering seasons. However, the potential effects of the presence of migratory birds in their wintering grounds on populations of resident birds have remain largely unexplored. Here, we propose the hypothesis that migratory birds negatively affect the habitat occupancy and population abundance of resident birds because of the arrival of numerous individuals during the most limiting months of the year. Here, we studied different species of migratory and resident birds that coexist during winter in an urban ecological reserve located within Mexico City. We used single-species multiseason occupancy models, two-species occupancy models, and distance sampling techniques to evaluate changes in occupancy and population density of resident bird species during three consecutive winters. We found an aggregation pattern between two resident species (Psaltriparus minimus and Thryomanes bewickii) with three migratory warblers (Cardellina pusilla, Setophaga coronata and Setophaga townsendi). Thus, our results provide evidence of the formation of mixed-species flocks in our study area. We also conclude that resident birds experience different demographic and behavioral processes during winter that not necessarily result from interspecific interactions with migratory birds.     

Henipavirus neutralising antibodies in an isolated island population of African fruit bats

Isolated islands provide valuable opportunities to study the persistence of viruses in wildlife populations, including population size thresholds such as the critical community size. The straw-coloured fruit bat, Eidolon helvum, has been identified as a reservoir for henipaviruses (serological evidence) and Lagos bat virus (LBV; virus isolation and serological evidence) in continental Africa. Here, we sampled from a remote population of E. helvum annobonensis fruit bats on Annobón island in the Gulf of Guinea to investigate whether antibodies to these viruses also exist in this isolated subspecies. Henipavirus serological analyses (Luminex multiplexed binding and inhibition assays, virus neutralisation tests and western blots) and lyssavirus serological analyses (LBV: modified Fluorescent Antibody Virus Neutralisation test, LBV and Mokola virus: lentivirus pseudovirus neutralisation assay) were undertaken on 73 and 70 samples respectively. Given the isolation of fruit bats on Annobón and their lack of connectivity with other populations, it was expected that the population size on the island would be too small to allow persistence of viruses that are thought to cause acute and immunising infections. However, the presence of antibodies against henipaviruses was detected using the Luminex binding assay and confirmed using alternative assays. Neutralising antibodies to LBV were detected in one bat using both assays. We demonstrate clear evidence for exposure of multiple individuals to henipaviruses in this remote population of E. helvum annobonensis fruit bats on Annobón island. The situation is less clear for LBV. Seroprevalences to henipaviruses and LBV in Annobón are notably different to those in E. helvum in continental locations studied using the same sampling techniques and assays. Whilst cross-sectional serological studies in wildlife populations cannot provide details on viral dynamics within populations, valuable information on the presence or absence of viruses may be obtained and utilised for informing future studies.