Trachops Research Articles

Análisis filogenético del género Mimon Gray, 1847 (Mammalia, Chiroptera, Phyllostomidae) con la descripción de un nuevo género

Introduction: Mimon is currently considered a monophyletic genus that comprises two subgenera: Mimon (represented by M. bennettii and M. cozumelae ), and the taxon formerly named “ Anthorhina ” (represented by M. crenulatum and M. koepckeae ). However, recent molecular phylogenies show Mimon as a polyphyletic genus within Phyllostomidae. Methods: Herein, we present a phylogenetic approach based on morphology, which includes all species of the genus Mimon , with emphasis on geographical populations of M. crenulatum . Our data matrix was built with our own examination of M. bennetti ( n = 5), M. cozumelae ( n = 31), M. crenulatum ( n = 181), and M. koepckeae ( n = 3) for 91 morphological characters including external, skull-dental and postcraneal traits. The species Lophostoma occidentalis, Trachops cirrhosus, Tonatia saurophila, Phyllostomus discolor , Phylloderma stenops , and Micronycteris megalotis were selected as outgroups. The tree was rooted on M. megalotis . An exhaustive search with 135 unordered characters was performed to find the most parsimonious trees. Results: A single well-supported tree of 306 steps was obtained. Bootstrap and Jacknife with 10,000 resampling were used as support estimators. The most parsimonious tree confirms Mimon is a polyphyletic genus, where the subgenus Mimon and the taxon formerly named “ Anthorhina ” are strongly supported but unrelated monophyletic groups. Discussion and Conclusions: In order to solve this taxonomic problem, we recommend the taxon formerly named “ Anthorhina ” be raised at genus level, but with a new name because “ Anthorhina ” is a synonym of Tonatia . Finally, we provide an emended diagnosis of Mimon s.s. and the description of a new genus, based on morphological characters used for the phylogeny. Key words: Gardnerycteris nov. gen., morphological, maximun parsimony.

Risks of multimodal signaling: bat predators attend to dynamic motion in frog sexual displays.

Many sexual displays contain multiple components that are received through a variety of sensory modalities. Primary and secondary signal components can interact to induce novel receiver responses and become targets of sexual selection as complex signals. However, predators can also use these complex signals for prey assessment, which may limit the evolution of elaborate sexual signals. We tested whether a multimodal sexual display of the male túngara frog (Physalaemus pustulosus) increases predation risk from the fringe-lipped bat (Trachops cirrhosus) when compared with a unimodal display. We gave bats a choice to attack one of two frog models: a model with a vocal sac moving in synchrony with a mating call (multisensory cue), or a control model with the call but no vocal sac movement (unimodal cue). Bats preferred to attack the model associated with the multimodal display. Furthermore, we determined that bats perceive the vocal sac using echolocation rather than visual cues. Our data illustrate the costs associated with multimodal signaling and that sexual and natural selection pressures on the same trait are not always mediated through the same sensory modalities. These data are important when considering the role of environmental fluctuations on signal evolution as different sensory modalities will be differentially affected.

The Quaternary vertebrate fauna of the limestone cave Gruta do Ioiô, northeastern Brazil

The present study reports the Quaternary vertebrate fauna of Gruta do Ioiô, a partially submerged limestone cave located in central Bahia, northeastern Brazil. A semi-arid weather prevails nowadays in the area, which is mostly covered by a xeric low arboreal scrubland known as Caatinga. The identified taxa include: Rhamdia (Osteichtyes, Siluriformes), Caiman (Crocodyliformes, Caimaninae), Myocastor cf. Myocastor coypus (Rodentia, Myocastoridae), Holochilus sciureus (Rodentia, Sigmodontinae), Natalus cf. Natalus macrourus (Chiroptera, Natalidae), Tonatia bidens, Trachops cirrhosus (Chiroptera, Phyllostomidae), and Eira cf. Eira barbara (Carnivora, Mustelidae). Whereas Rhamdia and Caiman have scarce fossil records, the recovered mammals have already been reported from Quaternary localities of northeastern Brazil, although only two of them are present in the current local fauna. Taphonomic signatures and the nature of the fossiliferous site indicate that the vertebrates lived inside or nearby the cave, including the swamp by its main entrance. Radiocarbon dating of dental bioapatite yielded calibrated ages between 19,980 and 22,040 BP. This indicates that the accumulation started at least during the late Pleistocene, within the Last Glacial Maximum. In agreement with the mode of life of most taxa recognized here, previous studies indicated that this was a wetter period in the region.

Risky Ripples Allow Bats and Frogs to Eavesdrop on a Multisensory Sexual Display

Animal displays are often perceived by intended and unintended receivers in more than one sensory system. In addition, cues that are an incidental consequence of signal production can also be perceived by different receivers, even when the receivers use different sensory systems to perceive them. Here we show that the vocal responses of male túngara frogs (Physalaemus pustulosus) increase twofold when call-induced water ripples are added to the acoustic component of a rival's call. Hunting bats (Trachops cirrhosus) can echolocate this signal by-product and prefer to attack model frogs when ripples are added to the acoustic component of the call. This study illustrates how the perception of a signal by-product by intended and unintended receivers through different sensory systems generates both costs and benefits for the signaler.

Species composition and seasonal variation in abundance of Phyllostomidae bats (Chiroptera) in an Atlantic Forest remnant, southeastern Brazil

Normally, the Phyllostomidae bat community var- ies in number of individuals depending on food availability, which in turn varies with changes in annual rainfall. The aims of this study were to list species of Phyllostomidae bats in Curi o Municipal Natural Park located in the munici- pality of Paracambi, state of Rio de Janeiro, southeastern Brazil, and determine possible differences in species rich- ness, abundance and composition between rainy and dry seasons. Sampling was carried out between September 2011 and August 2012 with the use of mist nets. The total sampling effort was 51,840 m 2 h, and 745 individuals of 18 bat species were caught. Myotis riparius (Vespertilionidae) was the only non-Phyllostomidae species caught. Artibeus lituratus and Carollia perspicillata were the most abundant species. The collector curve did not become stabilized, with 21 ± 2 phyllostomid species being estimated for the park. No significant difference in species richness or change in the community composition was found between seasons; how- ever a higher number of individuals was captured in the rainy season. The occurrence of specie indicator of good- quality habitats ( Chrotopterus auritus , Micronycteris micro- tis and Trachops cirrhosus ) and species threatened with extinction ( Chiroderma doriae and Dermanura cinerea ) indicate that the park is an important forest remnant for the conservation of bats and needs to be monitored.

Population and seasonal variation in response to prey calls by an eavesdropping bat

The fringe-lipped bat, Trachops cirrhosus, is an eavesdropping predator that hunts frogs and katydids by approaching these preys' sexual advertisement calls. In captivity, bats can rapidly learn to associate novel acoustic stimuli with food rewards. It is unknown how this learning ability is related to foraging behavior in the wild where prey and the calls that identify them vary over space and time. In two bat populations that differ in available prey species (Soberania, Panama, and La Selva, Costa Rica), we presented wild-caught bats with frog calls, katydid calls, and control stimuli. Bats in Soberania were significantly more responsive to complex calls and choruses of the tungara frog, Physalaemus pustulosus, than were bats in La Selva. La Selva bats were significantly more responsive to katydid calls (Steirodon sp.) than Soberania bats. We also examined seasonal variation in bat response to prey cues. Bats were captured in Soberania in dry and wet seasons and presented with the calls of a dry season breeding frog (Smilisca sila), a wet season breeding frog (P. pustulosus), and four katydid species. Bats captured in the dry season were significantly more responsive to the calls of S. sila than bats captured in the wet season, but there were no seasonal differences in response to the calls of P. pustulosus or the katydid calls. We demonstrate plasticity in the foraging behavior of this eavesdropping predator but also show that response to prey cues is not predicted solely by prey availability.

When to approach novel prey cues? Social learning strategies in frog-eating bats

Animals can use different sources of information when making decisions. Foraging animals often have access to both self-acquired and socially acquired information about prey. The fringe-lipped bat, Trachops cirrhosus, hunts frogs by approaching the calls that frogs produce to attract mates. We examined how the reliability of self-acquired prey cues affects social learning of novel prey cues. We trained bats to associate an artificial acoustic cue (mobile phone ringtone) with food rewards. Bats were assigned to treatments in which the trained cue was either an unreliable indicator of reward (rewarded 50% of the presentations) or a reliable indicator (rewarded 100% of the presentations), and they were exposed to a conspecific tutor foraging on a reliable (rewarded 100%) novel cue or to the novel cue with no tutor. Bats whose trained cue was unreliable and who had a tutor were significantly more likely to preferentially approach the novel cue when compared with bats whose trained cue was reliable, and to bats that had no tutor. Reliability of self-acquired prey cues therefore affects social learning of novel prey cues by frog-eating bats. Examining when animals use social information to learn about novel prey is key to understanding the social transmission of foraging innovations.

Do frog-eating bats perceptually bind the complex components of frog calls?

The mating calls of male túngara frogs, Physalaemus pustulosus, attract intended (conspecific females) and unintended (eavesdropping predators and parasites) receivers. The calls are complex, having two components: a frequency-modulated "whine" followed by 0-7 harmonic bursts or "chucks". The whine is necessary and sufficient to elicit phonotaxis from females and the chuck enhances call attractiveness when it follows a whine. Although chucks are never made alone, females perceptually bind the whine and chuck when they are spatially separated. We tested whether an unintended receiver with independent evolution of phonotaxis, the frog-eating bat, Trachops cirrhosus, has converged with frogs in its auditory grouping of the call components. In contrast to frogs, bats approached chucks broadcast alone; when the chuck was spatially separated from the whine the bats preferentially approached the whine, and bats were sensitive to whine-chuck temporal sequence. This contrast suggests that although disparate taxa may be selected to respond to the same signals, different evolutionary histories, selective regimes, and neural and cognitive architectures may result in different weighting and grouping of signal components between generalist predators and conspecific mates.

Echolocation intensity and directionality of perching and flying fringe-lipped bats, Trachops cirrhosus (Phyllostomidae)

The Neotropical frog-eating bat, Trachops cirrhosus, primarily hunts stationary prey, either by gleaning on the wing, or in a sit-and-wait mode hanging from a perch. It listens passively for prey-generated sounds, but uses echolocation in all stages of the hunt. Like other bats in the family Phyllostomidae, T. cirrhosus has a conspicuous nose leaf, hypothesized to direct and focus echolocation calls emitted from the nostrils. T. cirrhosus is highly flexible in its cognitive abilities and its use of sensory strategies for prey detection. Additionally, T. cirrhosus has been observed to echolocate both with closed and open mouth. We hypothesize that its flexibility extends to echolocation call design. We investigated the effect of hunting mode, perching or flying, as well as the effect of mouth opening, on the acoustic parameters and directionality of the echolocation call. We used a multi-microphone array, a high-speed video camera, and a microphone-diode-video system to directly visualize the echolocation sound beam synchronized with the bat's behavior. We found that T. cirrhosus emits a highly directional sound beam with half amplitude angle (HAM) of 12–18° and DI (directionality index) of ~17 dB, among the most directional bat sonar beams measured to date. The directionality was high both when flying and when perching. The emitted intensity was low, around 88 dB SPL at 10 cm from the mouth, when hanging, but higher, around 100 dB SPL at 10 cm, when flying or just before take-off. Our data suggests that the limited search volume of T. cirrhosus sonar beam defined by the high directionality and the rather low intensity of its echolocation calls is adapted to the highly cluttered hunting habitat and to the perch hunting mode.

Comunidade de morcegos (Mammalia, Chiroptera) no Refúgio de Vida Silvestre Mata do Junco, Sergipe, nordeste do Brasil

A ordem Chiroptera é a segunda maior em riqueza de mamíferos no Brasil e a Mata Atlântica é o bioma com o melhor estado de conhecimento para esse grupo. Em Sergipe, estudos sobre quirópteros ainda são escassos, sendo necessário ampliar as pesquisas com esses animais. O presente trabalho teve como objetivo realizar o inventário de morcegos do Refúgio de Vida Silvestre Mata do Junco (RVSMJ), segunda maior reserva de Mata Atlântica do estado de Sergipe. As coletas foram realizadas durante duas noites por mês, entre fevereiro de 2011 a fevereiro de 2012, exceto junho. Com um esforço de captura de 21.168 m².h foram registrados 189 indivíduos de duas famílias e 14 espécies. Destas, Artibeus planirostris, Chiroderma doriae, Myotis nigricans, Phyllostomus discolor, Trachops cirrhosus e Trinycteris nicefori correspondem a novas ocorrências para a localidade, sendo T. nicefori novo registro para o estado. Phyllostomidae foi a família com maior riqueza e abundância e A. lituratus (N = 67), Carollia perspicillata (N = 45) e Dermanura cinerea (N = 45) foram as espécies mais abundantes. Essas três espécies juntas representam 83,0% dos indivíduos capturados; sendo caracterizadas como generalistas no uso do habitat e dieta. Com relação às guildas alimentares, a maioria das espécies é frugívora (57,1%), devido a metodologia e existência de áreas agrícolas presentes no RVSMJ. O registro de novas espécies para a localidade, juntamente com os parâmetros obtidos de riqueza, abundância e guilda alimentar, contribuem para o aumento do conhecimento dos quirópteros em Sergipe e podem servir de base para estratégias de conservação e manejo dessa área.

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.

Hematological Survey of Common Neotropical Bat Species from Costa Rica

Although bats are one of the largest groups within the class Mammalia and may carry several zoonotic diseases, basic information about their hematology is limited. In this study, hematocrit (Hct), total white blood cell counts (TWBC; leukocytes), and differential white blood cell counts (DWBC) of free-ranging Neotropical bats were quantified. Blood samples from 255 bats representing 26 species from the families of Emballonuridae (3 species; 33 individuals), Molossidae (2 species; 26 individuals), Mormoopidae (1 species; 1 individual), Phyllostomidae (18 species; 180 individuals), and Vespertilionidae (2 species; 15 individuals) were collected in a Caribbean lowland rainforest of Costa Rica. Hct was measured after centrifugation of microhematocrit capillaries, TWBCs were performed using the Unopette system and a hemocytometer, and DWBCs were performed on eosin methylene blue stained blood films. Hct of bats ranged between 51.8 +/- 0.7% for Phyllostomus discolor (n = 27) and 65.8 +/- 2.2% for Molossus sinaloae (n = 6). Bat species of the same taxonomic family had comparable TWBCs; these were lower for insectivorous emballonurid, molossid, and vespertilionid bat species than for mostly phytophagous phyllostomid bat species. However, Ectophylla alba (Phyllostomidae) exhibited exceptionally low TWBCs (836 +/- 166 /microl; n = 10); this was less than half of the TWBCs of all other bat species, which ranged from 1,714 +/- 297/microl for Molossus bondae (n = 20) to 7,339 +/- 1,503/microl for Trachops cirrhosus (n = 6). Species with higher TWBCs tended to have lower Hct values. Overall, blood cell morphology was similar to other mammalian species. A large number of polychromatophilic erythrocytes and differences in lymphocyte morphology were noted. This study provides important hematological values for Neotropical bat species and significantly expands the knowledge on basal physiological measurements of Chiroptera.

Observations on the Reproductive Behavior of a Neotropical Glassfrog,Hyalinobatrachium fleischmanni(Anura: Centrolenidae)

ABSTRACT. This study investigated geographic variation in a suite of reproductive behavioral traits in Hyalinobatrachium fleischmanni across several sites in Mexico and Ecuador. We made observations on the frequency of egg-mass brooding behavior and compared brooding encounter rates between wet and dry forest types. Brooding encounter rates were significantly higher in the drier region, suggesting a potential relationship between paternal care and climatic conditions. We also compared calling and oviposition sites between geographic regions and tested for associations with the distributional range of the frog-eating bat, Trachops cirrhosus. In regions where H. fleischmanni and T. cirrhosus co-occur, both calling males and egg masses were more frequently found on ‘less exposed’ lower surfaces of leaves, where risk of attack from aerial predators may be reduced. We also provide novel information on brooding behavior and clutch guarding, and discuss the implications of our results in the framework of existin...

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.

Comparative cytogenetic analysis between Lonchorhina aurita and Trachops cirrhosus (Chiroptera, Phyllostomidae)

Phyllostomidae comprises the most diverse family of neotropical bats, its wide range of morphological features leading to uncertainty regarding phylogenetic relationships. Seeing that cytogenetics is one of the fields capable of providing support for currently adopted classifications through the use of several markers, a comparative analysis between two Phyllostomidae species was undertaken in the present study, with a view to supplying datasets for the further establishment of Phyllostomidae evolutionary relationships. Karyotypes of Lonchorhina aurita (2n = 32; FN = 60) and Trachops cirrhosus (2n = 30; FN = 56) were analyzed by G- and C-banding, silver nitrate staining (Ag-NOR) and base-specific fluorochromes. Chromosomal data obtained for both species are in agreement with those previously described, except for X chromosome morphology in T. cirrhosus, hence indicating chromosomal geographical variation in this species. A comparison of G-banding permitted the identification of homeologies in nearly all the chromosomes. Furthermore, C-banding and Ag-NOR patterns were comparable to what has already been observed in the family. In both species CMA3 /DA/DAPI staining revealed an R-banding-like pattern with CMA 3 , whereas DAPI showed uniform staining in all the chromosomes. Fluorochrome staining patterns for pericentromeric constitutive heterochromatin (CH) regions, as well as for nucleolar organizing regions (NORs), indicated heterogeneity regarding these sequences among Phyllostomidae species.

The effect of signal complexity on localization performance in bats that localize frog calls

The fringe-lipped bat, Trachops cirrhosus, uses frog mating calls to detect and locate its prey. The tungara frog, Physalaemus pustulosus, a preferred prey species of this bat, produces two types of sexual advertise- ment calls, simple and complex, and both female frogs and predatory bats prefer complex calls to simple ones. Complex calls differ from simple ones in that they contain chucks: short, broadband suffixes with distinct onsets and offsets, acoustic properties that should maximize binaural comparisons and facilitate localization. We investigated the hypothesis that frog-eating bats prefer the complex calls of tungara frogs to simple ones because they find complex calls easier to localize. We tested bats under experimental con- ditions that mirror the conditions they encounter in nature: we broadcast tungara frog calls with and with- out background noise and with and without intervening obstacles. We broadcast calls either continuously during the hunting approach or only prior to the bat's flight to mimic the conditions under which frogs have detected an approaching bat and ceased calling. Bats showed a trend for better localization perfor- mance of complex calls than of simple ones under all treatment conditions. We found significant differ- ences in localization performance in some but not all levels of localization task complexity. This study is the first to offer evidence that an eavesdropping predator shows better localization performance for a pre- ferred signal variant of its prey.

Echolocating bats control the directionality of sonar signals to sort out the auditory scene

A primary function of hearing is the localization and identification of sound sources in the auditory scene. Results from humans and other animals have shown that spectral and temporal features, as well as source direction, are important parameters used for organizing acoustic sources. Echolocating bats control the features of vocalizations to shape information carried by echoes from auditory objects. Our research on big brown bats, Eptesicus fuscus, suggests the importance of vocal control for scene analysis: When a bat performs a dual task, requiring both obstacle avoidance and prey capture, it solves the task sequentially, adapting the temporal pattern of its cries to produce sonar strobe groups, strobing first the obstacle and then the prey. Directional control over the sonar beam pattern confirms this sequential processing: The bat alternates fixation of the beam axis on the obstacle and prey. The importance of directionality is corroborated by studies in another bat, Trachops cirrhosus, where behavior and morphology optimize sonar directionality for different tasks. When hanging from a perch T. cirrhosus emits sounds for general orientation with limited demands for directionality. When hunting, prey localization necessitates high directionality associated with sound emission through the nostrils surrounded by the moveable nose leaf.

Acoustic preferences and localization performance of blood-sucking flies (Corethrella Coquillett) to túngara frog calls

Mating signals that increase attractiveness of males to females can also increase conspicuousness of the signaler to predators and parasites. We investigated the acoustic preference of species of blood-sucking flies of the genus Corethrella (Diptera: Corethrelli- dae), which eavesdrop on the sexual advertisement signals of tungara frogs (Physalaemus pustulosus). Male frogs of this species facultatively produce 2 types of mating calls: simple (whines alone) and complex (whines and chucks). We tested the acoustic preference of the flies and their ability to locate their host when the frogs produce simple or complex calls. The flies exhibited phonotaxis to both types of calls but were preferentially attracted to complex calls. We show that acoustic information alone is sufficient for the flies' accurate localization of calling frogs. Complex calls, however, were not approached at closer distance or with decreased landing error (i.e., proportion of landings outside the target) than simple calls, suggesting that call structure does not influence localization performance. Female tungara frogs and frog-eating bats (Trachops cirrhosus) also prefer com- plex to simple tungara frog calls. Thus, intended and unintended receivers with different ear morphologies exhibit the same preference for a specific tungara frog call type. This result is discussed in the context of the evolution of call attractiveness in a communication network. Key words: acoustic communication, communication network, host-parasite interaction, sound localization. (Behav Ecol)

Social Transmission of Novel Foraging Behavior in Bats: Frog Calls and Their Referents

The fringe-lipped bat, Trachops cirrhosus, uses prey-emitted acoustic cues (frog calls) to assess prey palatability . Previous experiments show that wild T. cirrhosus brought into the laboratory are flexible in their ability to reverse the associations they form between prey cues and prey quality . Here we asked how this flexibility can be achieved in nature. We quantified the rate at which bats learned to associate the calls of a poisonous toad species with palatable prey by placing bats in three groups: (a) social learning, in which a bat inexperienced with the novel association was allowed to observe an experienced bat; (b) social facilitation, in which two inexperienced bats were presented with the experimental task together; and (c) trial-and-error, in which a single inexperienced bat was presented with the experimental task alone. In the social-learning group, bats rapidly acquired the novel association in an average of 5.3 trials. In the social-facilitation and trial-and-error groups, most bats did not approach the call of the poisonous species after 100 trials. Thus, once acquired, novel associations between prey cue and prey quality could spread rapidly through the bat population by cultural transmission. This is the first case to document predator social learning of an acoustic prey cue.

Animal Behavior: Who Will Croak Next?

A recent study with the predatory bat Trachops cirrhosus has shown the importance for this species of social learning about novel prey using auditory, rather than visual or olfactory, cues.