Sensory challenges for trawling bats: Finding transient prey on water surfaces.

Bats are able to identify obstacles and prey objects based exclusively on acoustic information acquired via echolocation. To assess the echo information potentially available to the trawling bat Noctilio leporinus, prey objects were ensonified with artificial bat calls and deduced echo target strengths (TS) of the reflected signals. The artificial calls consisted either of constant frequency (CF) or frequency modulated (FM) sounds. Detection distances were calculated for call intensities of N. leporinus emitted in the field and in confined space. Measurements of a transient target consisting of a brief water splash and subsequently expanding water ripples revealed that concentrically expanding water ripples can provide sufficiently loud echoes to be detected by trawling bats. Experiments with stationary targets revealed differences in TS depending on the type of signal used (CF or FM). A calculated maximum detection distance between 4.5 and 13.7 m for all measured targets indicates that prey detection in this very loud calling species occurs much earlier than suggested by estimations based on modifications in echolocation or flight behavior.

Sensory-based niche partitioning in a multiple predator - multiple prey community.

Many predators and parasites eavesdrop on the communication signals of their prey. Eavesdropping is typically studied as dyadic predator-prey species interactions; yet in nature, most predators target multiple prey species and most prey must evade multiple predator species. The impact of predator communities on prey signal evolution is not well understood. Predators could converge in their preferences for conspicuous signal properties, generating competition among predators and natural selection on particular prey signal features. Alternatively, predator species could vary in their preferences for prey signal properties, resulting in sensory-based niche partitioning of prey resources. In the Neotropics, many substrate-gleaning bats use the mate-attraction songs of male katydids to locate them as prey. We studied mechanisms of niche partitioning in four substrate-gleaning bat species and found they are similar in morphology, echolocation signal design and prey-handling ability, but each species preferred different acoustic features of male song in 12 sympatric katydid species. This divergence in predator preference probably contributes to the coexistence of many substrate-gleaning bat species in the Neotropics, and the substantial diversity in the mate-attraction signals of katydids. Our results provide insight into how multiple eavesdropping predator species might influence prey signal evolution through sensory-based niche partitioning.

Cheating on the mutualistic contract: nutritional gain through seed predation in the frugivorous bat Chiroderma villosum (Phyllostomidae).

Most frugivorous bats are efficient seed dispersers, as they typically do not damage seeds and transport them over long distances. In contrast, bats of the phyllostomid genus Chiroderma cheat fig trees by acting more as seed predators than as seed dispersers. The bats initially separate seeds from fruit pulp in the mouth. After extracting the juice from the fruit pulp, they thoroughly chew the seeds and spit out small seed fragments in a pellet. Consequently, the faeces contain almost no viable seeds. We compared the nutrient content of intact fig seeds with ejecta and faecal samples from both Chiroderma villosum and the 'conventional' frugivorous bat Artibeus watsoni. We show that C. villosum can extract nutrients from the seeds, especially protein and fat. The processing time of figs showed no significant difference between the two bat species. Food-choice experiments showed that C. villosum preferred fig species with more seeds over those with fewer seeds. This preference, in combination with the specialized seed-chewing behaviour, leads to an increased nutrient intake per fig. This unique strategy enables C. villosum to satisfy its nutritional requirements with a lower number of figs than other species, which decreases the amount of energy necessary for foraging flights as well as the predation risk during foraging.

Species undersampling in tropical bat surveys: effects on emerging biodiversity patterns.

Undersampling is commonplace in biodiversity surveys of species-rich tropical assemblages in which rare taxa abound, with possible repercussions for our ability to implement surveys and monitoring programmes in a cost-effective way. We investigated the consequences of information loss due to species undersampling (missing subsets of species from the full species pool) in tropical bat surveys for the emerging patterns of species richness (SR) and compositional variation across sites. For 27 bat assemblage data sets from across the tropics, we used correlations between original data sets and subsets with different numbers of species deleted either at random, or according to their rarity in the assemblage, to assess to what extent patterns in SR and composition in data subsets are congruent with those in the initial data set. We then examined to what degree high sample representativeness (r ≥ 0·8) was influenced by biogeographic region, sampling method, sampling effort or structural assemblage characteristics. For SR, correlations between random subsets and original data sets were strong (r ≥ 0·8) with moderate (ca. 20%) species loss. Bias associated with information loss was greater for species composition; on average ca. 90% of species in random subsets had to be retained to adequately capture among-site variation. For nonrandom subsets, removing only the rarest species (on average c. 10% of the full data set) yielded strong correlations (r > 0·95) for both SR and composition. Eliminating greater proportions of rare species resulted in weaker correlations and large variation in the magnitude of observed correlations among data sets. Species subsets that comprised ca. 85% of the original set can be considered reliable surrogates, capable of adequately revealing patterns of SR and temporal or spatial turnover in many tropical bat assemblages. Our analyses thus demonstrate the potential as well as limitations for reducing survey effort and streamlining sampling protocols, and consequently for increasing the cost-effectiveness in tropical bat surveys or monitoring programmes. The dependence of the performance of species subsets on structural assemblage characteristics (total assemblage abundance, proportion of rare species), however, underscores the importance of adaptive monitoring schemes and of establishing surrogate performance on a site by site basis based on pilot surveys.

Complementary ecosystem services provided by pest predators and pollinators increase quantity and quality of coffee yields.

Wild animals substantially support crop production by providing ecosystem services, such as pollination and natural pest control. However, the strengths of synergies between ecosystem services and their dependencies on land-use management are largely unknown. Here, we took an experimental approach to test the impact of land-use intensification on both individual and combined pollination and pest control services in coffee production systems at Mount Kilimanjaro. We established a full-factorial pollinator and vertebrate exclosure experiment along a land-use gradient from traditional homegardens (agroforestry systems), shaded coffee plantations to sun coffee plantations (total sample size = 180 coffee bushes). The exclusion of vertebrates led to a reduction in fruit set of ca 9%. Pollinators did not affect fruit set, but significantly increased fruit weight of coffee by an average of 7.4%. We found no significant decline of these ecosystem services along the land-use gradient. Pest control and pollination service were thus complementary, contributing to coffee production by affecting the quantity and quality of a major tropical cash crop across different coffee production systems at Mount Kilimanjaro.

The third dimension of bat migration: evidence for elevational movements of Miniopterus natalensis along the slopes of Mount Kilimanjaro.

Bats are important ecosystem service providers, and therefore most relevant for both lowland and highland habitats, particularly in the tropics. Yet, it is poorly understood to what extent they perform large-scale movements, especially movements along mountain slopes. Here, we studied the movement ecology of the potentially migratory species Miniopterus natalensis at Mount Kilimanjaro in Tanzania. We analysed stable isotope ratios of C (δ(13)C), N (δ(15)N) and H (δ(2)H) in keratin of sedentary frugivorous and insectivorous bats captured between 800 and 2,400 m above sea level to establish elevational gradients of stable isotope ratios in consumer tissues. We expected correlations between stable isotope ratios of the non-exchangeable portion of H in fur keratin and the elevation of capture site, but not necessarily for δ(13)C and δ(15)N. Yet, in bats of both feeding ensembles, we found δ(15)N of fur keratin to correlate positively with the elevation of capture sites but not δ(2)H. In frugivorous bats, δ(13)C increased with increasing capture elevation as well. By looking at intra-individual variation of δ(13)C and δ(15)N in fur keratin and wing membrane tissues of sedentary Rhinolophus cf. clivosus and of the potentially migratory species M. natalensis, we gathered evidence that M. natalensis migrates seasonally between low and high elevations along the slopes of Mount Kilimanjaro. Finally, based on an isoscape origin model we estimated that M. natalensis captured before and after the cold period at around 1,800 m above sea level originated from around 1,400 m a.s.l. or lower. Thus, we received convergent results in support of seasonal elevational movements of M. natalensis, probably in search for cold hibernacula at higher elevations of Mount Kilimanjaro.

Human betacoronavirus 2c EMC/2012-related viruses in bats, Ghana and Europe.

We screened fecal specimens of 4,758 bats from Ghana and 272 bats from 4 European countries for betacoronaviruses. Viruses related to the novel human betacoronavirus EMC/2012 were detected in 46 (24.9%) of 185 Nycteris bats and 40 (14.7%) of 272 Pipistrellus bats. Their genetic relatedness indicated EMC/2012 originated from bats.

Highly diversified coronaviruses in neotropical bats.

Bats host a broad diversity of coronaviruses (CoVs), including close relatives of human pathogens. There is only limited data on neotropical bat CoVs. We analysed faecal, blood and intestine specimens from 1562 bats sampled in Costa Rica, Panama, Ecuador and Brazil for CoVs by broad-range PCR. CoV RNA was detected in 50 bats representing nine different species, both frugivorous and insectivorous. These bat CoVs were unrelated to known human or animal pathogens, indicating an absence of recent zoonotic spill-over events. Based on RNA-dependent RNA polymerase (RdRp)-based grouping units (RGUs) as a surrogate for CoV species identification, the 50 viruses represented five different alphacoronavirus RGUs and two betacoronavirus RGUs. Closely related alphacoronaviruses were detected in Carollia perspicillata and C. brevicauda across a geographical distance exceeding 5600 km. Our study expands the knowledge on CoV diversity in neotropical bats and emphasizes the association of distinct CoVs and bat host genera.

Perception of silent and motionless prey on vegetation by echolocation in the gleaning bat Micronycteris microtis.

Gleaning insectivorous bats that forage by using echolocation within dense forest vegetation face the sensorial challenge of acoustic masking effects. Active perception of silent and motionless prey in acoustically cluttered environments by echolocation alone has thus been regarded impossible. The gleaning insectivorous bat Micronycteris microtis however, forages in dense understory vegetation and preys on insects, including dragonflies, which rest silent and motionless on vegetation. From behavioural experiments, we show that M. microtis uses echolocation as the sole sensorial modality for successful prey perception within a complex acoustic environment. All individuals performed a stereotypical three-dimensional hovering flight in front of prey items, while continuously emitting short, multi-harmonic, broadband echolocation calls. We observed a high precision in target localization which suggests that M. microtis perceives a detailed acoustic image of the prey based on shape, surface structure and material. Our experiments provide, to our knowledge, the first evidence that a gleaning bat uses echolocation alone for successful detection, classification and precise localization of silent and motionless prey in acoustic clutter. Overall, we conclude that the three-dimensional hovering flight of M. microtis in combination with a frequent emission of short, high-frequency echolocation calls is the key for active prey perception in acoustically highly cluttered environments.

Bats worldwide carry hepatitis E virus-related viruses that form a putative novel genus within the family Hepeviridae.

Hepatitis E virus (HEV) is one of the most common causes of acute hepatitis in tropical and temperate climates. Tropical genotypes 1 and 2 are associated with food-borne and waterborne transmission. Zoonotic reservoirs (mainly pigs, wild boar, and deer) are considered for genotypes 3 and 4, which exist in temperate climates. In view of the association of several zoonotic viruses with bats, we analyzed 3,869 bat specimens from 85 different species and from five continents for hepevirus RNA. HEVs were detected in African, Central American, and European bats, forming a novel phylogenetic clade in the family Hepeviridae. Bat hepeviruses were highly diversified and comparable to human HEV in sequence variation. No evidence for the transmission of bat hepeviruses to humans was found in over 90,000 human blood donations and individual patient sera. Full-genome analysis of one representative virus confirmed formal classification within the family Hepeviridae. Sequence- and distance-based taxonomic evaluations suggested that bat hepeviruses constitute a distinct genus within the family Hepeviridae and that at least three other genera comprising human, rodent, and avian hepeviruses can be designated. This may imply that hepeviruses invaded mammalian hosts nonrecently and underwent speciation according to their host restrictions. Human HEV-related viruses in farmed and peridomestic animals might represent secondary acquisitions of human viruses, rather than animal precursors causally involved in the evolution of human HEV.

Environmental factors affect Acidobacterial communities below the subgroup level in grassland and forest soils.

In soil, Acidobacteria constitute on average 20% of all bacteria, are highly diverse, and are physiologically active in situ. However, their individual functions and interactions with higher taxa in soil are still unknown. Here, potential effects of land use, soil properties, plant diversity, and soil nanofauna on acidobacterial community composition were studied by cultivation-independent methods in grassland and forest soils from three different regions in Germany. The analysis of 16S rRNA gene clone libraries representing all studied soils revealed that grassland soils were dominated by subgroup Gp6 and forest soils by subgroup Gp1 Acidobacteria. The analysis of a large number of sites (n = 57) by 16S rRNA gene fingerprinting methods (terminal restriction fragment length polymorphism [T-RFLP] and denaturing gradient gel electrophoresis [DGGE]) showed that Acidobacteria diversities differed between grassland and forest soils but also among the three different regions. Edaphic properties, such as pH, organic carbon, total nitrogen, C/N ratio, phosphorus, nitrate, ammonium, soil moisture, soil temperature, and soil respiration, had an impact on community composition as assessed by fingerprinting. However, interrelations with environmental parameters among subgroup terminal restriction fragments (T-RFs) differed significantly, e.g., different Gp1 T-RFs correlated positively or negatively with nitrogen content. Novel significant correlations of Acidobacteria subpopulations (i.e., individual populations within subgroups) with soil nanofauna and vascular plant diversity were revealed only by analysis of clone sequences. Thus, for detecting novel interrelations of environmental parameters with Acidobacteria, individual populations within subgroups have to be considered.

Climate, habitat, and species interactions at different scales determine the structure of a Neotropical bat community.

Climate, habitat, and species interactions are factors that control community properties (e.g., species richness, abundance) across various spatial scales. Usually, researchers study how a few properties are affected by one factor in isolation and at one scale. Hence, there are few multi-scale studies testing how multiple controlling factors simultaneously affect community properties at different scales. We ask whether climate, habitat structure, or insect resources at each of three spatial scales explains most of the variation in six community properties and which theory best explains the distribution of selected community properties across a rainfall gradient. We studied a Neotropical insectivorous bat ensemble in the Isthmus of Panama with acoustic monitoring techniques. Using climatological data, habitat surveys, and insect captures in a hierarchical sampling design we determined how much variation of the community properties was explained by the three factors employing two approaches for variance partitioning. Our results revealed that most of the variation in species richness, total abundance, and feeding activity occurred at the smallest spatial scale and was explained by habitat structure. In contrast, climate at large scales explained most of the variation in individual species' abundances. Although each species had an idiosyncratic response to the gradient, species richness peaked at intermediate levels of precipitation, whereas total abundance was very similar across sites, suggesting density compensation. All community properties responded in a different manner to the factor and scale under consideration.

Anonymous and EST-based microsatellite DNA markers that transfer broadly across the fig tree genus (Ficus, Moraceae).

PREMISE OF THE STUDY: We developed a set of microsatellite markers for broad utility across the species-rich pantropical tree genus Ficus (fig trees). The markers were developed to study population structure, hybridization, and gene flow in neotropical species. METHODS AND RESULTS: We developed seven novel primer sets from expressed sequence tag (EST) libraries of F. citrifolia and F. popenoei (subgen. Urostigma sect. Americana) and optimized five previously developed anonymous loci for cross-species amplification. The markers were successfully tested on four species from the basal subgenus Pharmacosycea sect. Pharmacosycea (F. insipida, F. maxima, F. tonduzii, and F. yoponensis) and seven species of the derived subgenus Urostigma (F. citrifolia, F. colubrinae, F. costaricana, F. nymphaeifolia, F. obtusifolia, F. pertusa, and F. popenoei). The 12 markers amplified consistently and displayed polymorphism in all the species. CONCLUSIONS: This set of microsatellite markers is transferable across the phylogenetic breadth of Ficus, and should therefore be useful for studies of population structure and gene flow in approximately 750 fig species worldwide.

Sequential assessment of prey through the use of multiple sensory cues by an eavesdropping bat.

Predators are often confronted with a broad diversity of potential prey. They rely on cues associated with prey quality and palatability to optimize their hunting success and to avoid consuming toxic prey. Here, we investigate a predator's ability to assess prey cues during capture, handling, and consumption when confronted with conflicting information about prey quality. We used advertisement calls of a preferred prey item (the túngara frog) to attract fringe-lipped bats, Trachops cirrhosus, then offered palatable, poisonous, and chemically manipulated anurans as prey. Advertisement calls elicited an attack response, but as bats approached, they used additional sensory cues in a sequential manner to update their information about prey size and palatability. While both palatable and poisonous small anurans were readily captured, large poisonous toads were approached but not contacted suggesting the use of echolocation for assessment of prey size at close range. Once prey was captured, bats used chemical cues to make final, post-capture decisions about whether to consume the prey. Bats dropped small, poisonous toads as well as palatable frogs coated in toad toxins either immediately or shortly after capture. Our study suggests that echolocation and chemical cues obtained at close range supplement information obtained from acoustic cues at long range. Updating information about prey quality minimizes the occurrence of costly errors and may be advantageous in tracking temporal and spatial fluctuations of prey and exploiting novel food sources. These findings emphasize the sequential, complex nature of prey assessment that may allow exploratory and flexible hunting behaviors.

The effects of reproductive state on digestive efficiency in three sympatric bat species of the same guild.

The functional link between food as an energy source and metabolizable energy is the digestive tract. The digestive organs may change in size, structure, or retention time in response to energetic demands of the animal. Very efficient digestive tracts may be better at processing food but require higher energetic investments for maintenance even when post-absorptive. These costs influence the resting metabolic rate (RMR) that is defined as the energy necessary to fuel vital metabolic functions in a resting animal. In bats a trade-off between the necessity for a highly efficient digestive tract and moderate energetic maintenance costs may be particularly important. We hypothesized that low RMR coincides with low digestive efficiency (defined as apparent metabolizable energy coefficient (MEC)) and that phases of increased energetic demand are compensated for by increased digestive efficiency. We measured RMR and apparent MEC in the bats species Myotis nattereri, M. bechsteinii, and Plecotus auritus. In support of our hypothesis, M. nattereri has the lowest mass-specific RMR of the three species and the lowest apparent MEC. However, apparent MEC did not change during phases with differing energetic demands in any of the bat species, probably because bats operate at the limit of their sustainable energy demand.

Frequency alternation and an offbeat rhythm indicate foraging behavior in the echolocating bat, Saccopteryx bilineata.

The greater sac-winged bat, Saccopteryx bilineata (Emballonuridae), uses two distinct echolocation call sequences: a 'monotonous' sequence, where bats emit ~48 kHz calls at a relatively stable rate, and a frequency-alternating sequence, where bats emit calls at ~45 kHz (low-note call) and ~48 kHz (high-note call). The frequencies of these low-high-note pairs remain stable within sequences. In Panama, we recorded echolocation calls from S. bilineata with a multi-microphone array at two sites: one a known roosting site, the other a known foraging site. Our results indicate that this species (1) only produces monotonous sequences in non-foraging contexts and, at times, directly after emitting a feeding buzz and (2) produces frequency-alternating sequences when actively foraging. These latter sequences are also characterized by an unusual, offbeat emission rhythm. We found significant positive relationships between (1) call intensity and call duration and (2) call intensity and distance from clutter. However, these relationships were weaker than those reported for bats from other families. We speculate on how call frequency alternation and an offbeat emission rhythm might reflect a novel strategy for prey detection at the edge of complex habitat in this ancient family of bats.

Echolocation call intensity and directionality in flying short-tailed fruit bats, Carollia perspicillata (Phyllostomidae).

The directionality of bat echolocation calls defines the width of bats' sonar "view," while call intensity directly influences detection range since adequate sound energy must impinge upon objects to return audible echoes. Both are thus crucial parameters for understanding biosonar signal design. Phyllostomid bats have been classified as low intensity or "whispering bats," but recent data indicate that this designation may be inaccurate. Echolocation beam directionality in phyllostomids has only been measured through electrode brain-stimulation of restrained bats, presumably excluding active beam control via the noseleaf. Here, a 12-microphone array was used to measure echolocation call intensity and beam directionality in the frugivorous phyllostomid, Carollia perspicillata, echolocating in flight. The results showed a considerably narrower beam shape (half-amplitude beam angles of approximately 16° horizontally and 14° vertically) and louder echolocation calls [source levels averaging 99 dB sound pressure level (SPL) root mean square] for C. perspicillata than was found for this species when stationary. This suggests that naturally behaving phyllostomids shape their sound beam to achieve a longer and narrower sonar range than previously thought. C. perspicillata orient and forage in the forest interior and the narrow beam might be adaptive in clutter, by reducing the number and intensity of off-axis echoes.

Auditory-based defence against gleaning bats in neotropical katydids (Orthoptera: Tettigoniidae).

Neotropical katydids (Orthoptera: Tettigoniidae) are preyed on by gleaning bats, which are known to use male calling songs to locate them. At least one katydid species has been reported to stop singing in response to bat echolocation calls. To investigate the relationship between this behavioural defence and ecological and sensory factors, we surveyed calling song characteristics, song cessation in response to the echolocation calls of a sympatric gleaning bat (Trachops cirrhosus), and T-cell responses (an auditory interneuron sensitive to ultrasound) in five katydid species from Panamá. The two katydid species that stopped singing in response to bat calls (Balboa tibialis and Ischnomela gracilis, Pseudophyllinae) also had the highest T-cell spike number and rate in response to these stimuli. The third pseudophylline species (Docidocercus gigliotosi) did not reliably cease singing and had low T-cell spiking activity. Neoconocephalus affinis (Copiphorinae) produced continuous calling song, possibly preventing males from hearing the bat during singing, and did not show a behavioural response despite high T-cell activity in response to bat calls. Steirodon rufolineatum (Phaneropterinae) did not cease singing and differed in T-cell activity compared to the other species. T-cell function might not be conserved in katydids, and evidence for this idea is discussed.

Behavioural and physiological consequences of male reproductive trade-offs in edible dormice (Glis glis).

Testosterone mediates male reproductive trade-offs in vertebrates including mammals. In male edible dormice (Glis glis), reproductivity linked to high levels of testosterone reduces their ability to express torpor, which may be expected to dramatically increase thermoregulatory costs. Aims of this study were therefore to analyse behavioural and physiological consequences of reproductive activity in male edible dormice under ecologically and evolutionary relevant conditions in the field. As we frequently encountered sleeping groups in the field, we hypothesized that social thermoregulation should be an important measure to reduce energy expenditure especially in sexually active male edible dormice. Our results revealed that the occurrence of sleeping groups was negatively influenced by male body mass but not by reproductive status or ambient temperature. In reproductive as in non-reproductive males, the number of individuals huddling together was negatively influenced by their body mass. Thus in general males with a high body mass were sitting in smaller groups than males with a low body mass. However, in reproductive males group size was further negatively affected by ambient temperature and positively by testes size. Thus breeders formed larger sleeping groups at lower ambient temperatures and males with larger testes were found in larger groups than males with smaller testes. Measurements of oxygen consumption demonstrated that grouping behaviour represents an efficient strategy to reduce energy expenditure in edible dormice as it reduced energy requirements by almost 40%. In summary, results of this field study showcase how sexually active male edible dormice may, through behavioural adjustment, counterbalance high thermoregulatory costs associated with reproductive activity.

Effects of ingestion by neotropical bats on germination parameters of native free-standing and strangler figs (Ficus sp., Moraceae).

Fruit-eating animals can influence the germination success of seeds through transportation and handling. We experimentally tested the contribution of ingestion by the common fruit-eating bat, Artibeus jamaicensis (Phyllostomidae, Chiroptera), to the percentage and rate of seed germination of figs (Ficus, Moraceae), which are considered keystone species for many frugivores. We collected fruits from three species of native free-standing figs (subgenus Pharmacosycea: F. insipida, F. maxima and F. yoponensis) and three species of native strangler figs (subgenus Urostigma: F. nymphiifolia, F. obtusifolia and F. popenoei) on Barro Colorado Island, Panama. The germination success of seeds removed from fruit pulp either manually or by ingestion was very high (>92%), while seeds that were not removed from fruit pulp were destroyed by fast-growing fungi within a few days. The dynamics of seed germination were not influenced by ingestion, but differed between the two subgenera of figs. In free-standing figs, germination started significantly earlier (5.3 +/- 0.7 days) than in strangler figs (8.6 +/- 1.4 days). Furthermore, strangler seeds were covered with a sticky coating and their seedlings developed cotyledons faster than fine roots, in contrast to free-standing figs that showed the opposite pattern. Our results demonstrate that the germination of fig seeds is positively influenced by passage through the gut of A. jamaicensis. Furthermore, free-standing and strangler figs revealed differences in germination parameters that might be adaptive with respect to the suitability of microsites such as tree fall gaps or host trees for establishment.