Pteronotus Parnellii Research Articles

Quaternary Bats from the Impossível-Ioiô Cave System (Chapada Diamantina, Brazil): Humeral Remains and the First Fossil Record ofNoctilio leporinus(Chiroptera, Noctilionidae) from South America

The partially submerged Impossivel-Ioio cave system located in the karst region of Chapada Diamantina in Bahia (Brazil) has recently been the target of extensive paleontological studies. Here we provide the first report of fossil bats from this cave system, in which we recognize six species based on humeral remains: Furipterus horrens, Chrotopterus auritus, Mormoops cf. megalophylla, Pteronotus gymnonotus, Pteronotus parnellii, and Noctilio leporinus. Morphology of the humerus of these taxa is described in a comparative framework to document taxonomic assessments and provide a basis for future studies of fossil bat faunas. The relevance of the new records reported here is evaluated at a broader continental scale, as well as in contrast with the recent bat fauna of the region. The record of Noctilio leporinus stands as

Mitochondrial genome of the neotropical Parnell's mustached bat Pteronotus parnellii (Pteronotus, Mormoopidae)

We reported complete mitochondrial genome of neotropical Parnell's mustached bat Pteronotus parnellii (16,564 bp in length). Its mitochondrial genome consisted of 13 protein-coding genes, 22 transfer RNA genes, 2 ribosomal RNA genes and 1 control region. The base composition of mtDNA was A (33.1%), G (13.7%), C (27.3%), T (25.9%), and the percentage of A and T (59.0%) was higher than G and C. All the genes in P. parnellii were distributed on the H-strand, except for the ND6 subunit gene and 10 tRNA genes, which were encoded on the L-strand. The new sequenced mitochondrial genome will contribute to our understanding of the systematic evolution in the bats.

Resource partitioning by insectivorous bats in Jamaica.

In this investigation, we use variation in wing morphology, echolocation behaviour, patterns of habitat use and molecular diet analysis to demonstrate that six species of sympatric insectivorous bats in Jamaica show significant differences that could explain resource partitioning among the species. High-intensity echolocating species that used shorter, broadband signals and had shorter, broader wings (Pteronotus macleayii, Pteronotus quadridens, Mormoops blainvillii) foraged most in edge habitats, but differed in timing of peak activity. P. macleayii and M. blainvillii differed in diet, but low sample size precluded diet analysis for P. quadridens. High-intensity echolocating species that used longer, more narrowband signals and had longer, narrower wings (Molossus molossus, Tadarida brasiliensis) foraged most in open areas and differed in diet from the other species. Two disparate species were most active in clutter (dense vegetation). Pteronotus parnellii used high-duty-cycle echolocation apparently specialized for detecting fluttering targets in clutter. Macrotus waterhousii used low-intensity, broadband echolocation calls and presumably uses prey-generated sounds when foraging. These two species also differed in diet. Our data show that differences in morphology and echolocation behaviour coincide with differences in habitat use and diet, resulting in minimal overlap in resource use among species.

Blurry topography for precise target-distance computations in the auditory cortex of echolocating bats

Echolocating bats use the time from biosonar pulse emission to the arrival of echo (defined as echo delay) to calculate the space depth of targets. In the dorsal auditory cortex of several species, neurons that encode increasing echo delays are organized rostrocaudally in a topographic arrangement defined as chronotopy. Precise chronotopy could be important for precise target-distance computations. Here we show that in the cortex of three echolocating bat species (Pteronotus quadridens, Pteronotus parnellii and Carollia perspicillata), chronotopy is not precise but blurry. In all three species, neurons throughout the chronotopic map are driven by short echo delays that indicate the presence of close targets and the robustness of map organization depends on the parameter of the receptive field used to characterize neuronal tuning. The timing of cortical responses (latency and duration) provides a binding code that could be important for assembling acoustic scenes using echo delay information from objects with different space depths.

Neurons in the inferior colliculus of the mustached bat are tuned both to echo-delay and sound duration

Echolocation in bats requires a precise temporal processing of complex signals. This processing of time includes the encoding of echo-delay, which gives an estimation of target distance, and sound duration, which is considered to be important for own sound or echo recognition. In this study, we report that delay-tuned neurons in the inferior colliculus of the mustached bat (Pteronotus parnellii) are also tuned to sound duration. Collicular delay-tuned neurons showed three types of duration tuning: short-pass (12 of 64), band-pass (16 of 64), and long-pass (17 of 64). The remaining 19 delay-tuned neurons are not selective for sound duration. All short-pass and 10 band-pass neurons' characteristic delays were similar to characteristic duration. In six band-pass neurons, characteristic delay was different from characteristic duration. Neurons processing unmatched delay and durations could be participating in complex kinds of processing where the same neuron has different functions depending on the activated neural network.

High Duty Cycle to Low Duty Cycle: Echolocation Behaviour of the Hipposiderid Bat Coelops frithii

Laryngeally echolocating bats avoid self-deafening (forward masking) by separating pulse and echo either in time using low duty cycle (LDC) echolocation, or in frequency using high duty cycle (HDC) echolocation. HDC echolocators are specialized to detect fluttering targets in cluttered environments. HDC echolocation is found only in the families Rhinolophidae and Hipposideridae in the Old World and in the New World mormoopid, Pteronotus parnellii. Here we report that the hipposiderid Coelops frithii, ostensibly an HDC bat, consistently uses an LDC echolocation strategy whether roosting, flying, or approaching a fluttering target rotating at 50 to 80 Hz. We recorded the echolocation calls of free-flying C. frithii in the field in various situations, including presenting bats with a mechanical fluttering target. The echolocation calls of C. frithii consisted of an initial narrowband component (0.5±0.3 ms, 90.6±2.0 kHz) followed immediately by a frequency modulated (FM) sweep (194 to 113 kHz). This species emitted echolocation calls at duty cycles averaging 7.7±2.8% (n = 87 sequences). Coelops frithii approached fluttering targets more frequently than did LDC bats (C.frithii, approach frequency = 40.4%, n = 80; Myotis spp., approach frequency = 0%, n = 13), and at the same frequency as sympatrically feeding HDC species (Hipposideros armiger, approach rate = 53.3%, n = 15; Rhinolophus monoceros, approach rate = 56.7%, n = 97). We propose that the LDC echolocation strategy used by C. frithii is derived from HDC ancestors, that this species adjusts the harmonic contents of its echolocation calls, and that it may use both the narrowband component and the FM sweep of echolocations calls to detect fluttering targets.

Primer registro del murciélago bigotón <i>Pteronotus parnelli</i> (Chiroptera: Mormoopidae) al Este de Sonora

AbstractParnell’s mustached bat, Pteronotus parnellii, is found from southern Sonora and Tamaulipas to Chiapas in Mexico. On October 3, 2012, at 18:30 hr, six and nine-meter nets were placed above water ponds in the Babisal creek located in the “Northern Jaguar Reserve” near the town of Sahuaripa. At 19:50 hrs the six-meter net was checked, and an adult male, without scrotum, of the species Pteronotus parnellii was found at a height of 70cm above ground level. The Sahuaripa region in east-central Sonora, is outside the known distribution range of this species extending it by at least 220 km north of the Sierra de Alamos. The “Northern Jaguar Reserve” where Pteronotus parnellii was found, is a protected area and an important wilderness area for the protection of the northernmost breeding population of jaguars. Key words: Pteronotus parnellii, Reserva Jaguar del Norte, Sonora, october. Palabras clave: Pteronotus parnellii, Reserva Jaguar del Norte, Sonora, octubre.

Diversification and reproductive isolation: cryptic species in the only New World high-duty cycle bat, Pteronotus parnellii

BackgroundMolecular techniques are increasingly employed to recognize the presence of cryptic species, even among commonly observed taxa. Previous studies have demonstrated that bats using high-duty cycle echolocation may be more likely to speciate quickly. Pteronotus parnellii is a widespread Neotropical bat and the only New World species to use high-duty cycle echolocation, a trait otherwise restricted to Old World taxa. Here we analyze morphological and acoustic variation and genetic divergence at the mitochondrial COI gene, the 7th intron region of the y-linked Dby gene and the nuclear recombination-activating gene 2, and provide extensive evidence that P. parnellii is actually a cryptic species complex.ResultsCentral American populations form a single species while three additional species exist in northern South America: one in Venezuela, Trinidad and western Guyana and two occupying sympatric ranges in Guyana and Suriname. Reproductive isolation appears nearly complete (only one potential hybrid individual found). The complex likely arose within the last ~6 million years with all taxa diverging quickly within the last ~1-2 million years, following a pattern consistent with the geological history of Central and northern South America. Significant variation in cranial measures and forearm length exists between three of the four groups, although no individual morphological character can discriminate these in the field. Acoustic analysis reveals small differences (5–10 kHz) in echolocation calls between allopatric cryptic taxa that are unlikely to provide access to different prey resources but are consistent with divergence by drift in allopatric species or through selection for social recognition.ConclusionsThis unique approach, considering morphological, acoustic and multi-locus genetic information inherited maternally, paternally and bi-parentally, provides strong support to conclusions about the cessation of gene flow and degree of reproductive isolation of these cryptic species.

Evolution of neuronal mechanisms for echolocation: Specializations for target-range computation in bats of the genus Pteronotus

Delay tuning was studied in the auditory cortex of Pteronotus quadridens. All the 136 delay-tuned units that were studied responded strongly to heteroharmonic pulse-echo pairs presented at specific delays. In the heteroharmonic pairs, the first sonar call harmonic marks the timing of pulse emission while one of the higher harmonics (second or third) indicates the timing of the echo. Delay-tuned units are organized chronotopically along a rostrocaudal axis according to their characteristic delay. There is no obvious indication of multiple cortical axes specialized in the processing of different harmonic combinations of pulse and echo. Results of this study serve for a straight comparison of cortical delay-tuning between P. quadridens and the well-studied mustached bat, Pteronotus parnellii. These two species stem from the most recent and most basal nodes in the Pteronotus lineage, respectively. P. quadridens and P. parnellii use comparable heteroharmonic target-range computation strategies even though they do not use biosonar calls of a similar design. P. quadridens uses short constant-frequency (CF)/frequency-modulated (FM) echolocation calls, while P. parnellii uses long CF/FM calls. The ability to perform "heteroharmonic" target-range computations might be an ancestral neuronal specialization of the genus Pteronotus that was subjected to positive Darwinian selection in the evolution.

Diet of Mormoopid Bats on the Caribbean Island of Puerto Rico

Dietary differentiation can be a key mechanism for the coexistence of syntopic species with similar niches. On the Caribbean island of Puerto Rico, three species of bat from the family Mormoopidae — the Antillean ghost-faced bat (Mormoops blainvillei), sooty mustached bat (Pteronotus quadridens), and Parnell's mustached bat (Pteronotus parnellii portoricensis) — are aerial insectivores that roost in the same caves. To investigate the possibility of dietary differentiation, we estimated the percent volume and percent frequency of occurrence of the orders of arthropods consumed by these three species of bat, using standard fecal analysis. We also compared dietary diversity among species, as well as the amount of dietary overlap, with respect to season and habitat. Lastly, this study used canonical correspondence analysis (CCA), a method of ordination, to assess the effects of species, sex, age, reproductive condition, season, and habitat on intraspecific differences in the diet of the Puerto Rican Mormoopidae. Eight orders of arthropods were found in the diet of these mormoopids, with Lepidoptera, Hymenoptera, and Coleoptera being major staples. The CCA revealed differences in diet among the three species, suggesting that dietary differentiation is at least one mechanism for coexistence. In addition, the variables habitat and season correlated significantly with the diet of M. blainvillei and P. quadridens, whereas habitat and sex correlated with the diet of P. p. portoricensis. Thus, our study shows dietary differences among the three species of Mormoopidae living in the same caves on Puerto Rico, as well as intraspecific differences within the diet of each species.

Effects of anthropogenic disturbance and climate on patterns of bat fly parasitism.

Environmental conditions, including anthropogenic disturbance, can significantly alter host and parasite communities. Yet, our current knowledge is based mainly on endoparasites, while ectoparasites remain little studied. We studied the indirect effects of anthropogenic disturbance (human population density) and climate (temperature, precipitation and elevation) on abundance of highly host-specific bat flies in four Neotropical bat species across 43 localities in Venezuela. We formulated a set of 11 a priori hypotheses that included a combination of the two effectors and host species. Statistically, each of these hypotheses was represented by a zero-inflated negative binomial mixture model, allowing us to control for excess zeros in the data. The best model was selected using Akaike's information criteria. Fly abundance was affected by anthropogenic disturbance in Artibeus planirostris, Carollia perspicillata and Pteronotus parnellii, but not Desmodus rotundus. Climate affected fly abundance in all bat species, suggesting mediation of these effects via the host or by direct effects on flies. We conclude that human disturbance may play a role in shaping bat-bat fly interactions. Different processes could determine fly abundance in the different bat species.

Selectivity and persistent firing responses to social vocalizations in the basolateral amygdala

This study examined responsiveness to acoustic stimuli among neurons of the basolateral amygdala. While recording from single neurons in awake mustached bats (Pteronotus parnellii), we presented a wide range of acoustic stimuli including tonal, noise, and vocal signals. While many neurons displayed phasic or sustained responses locked to effective auditory stimuli, the majority of neurons (n=58) displayed a persistent excitatory discharge that lasted well beyond stimulus duration and filled the interval between successive stimuli. Persistent firing usually began seconds (median value, 5.4s) after the initiation of a train of repeated stimuli and lasted, in the majority of neurons, for at least 2min after the end of the stimulus train. Auditory-responsive amygdalar neurons were generally excited by one stimulus or very few stimuli. Most neurons did not respond well to synthetic stimuli including tones, noise bursts or frequency-modulated sweeps, but instead responded only to vocal stimuli (82 of 87 neurons). Furthermore, most neurons were highly selective among vocal stimuli. On average, neurons responded to 1.7 of 15 different syllables or syllable sequences. The largest percentage of neurons responded to a hiss-like rectangular broadband noise burst (rBNB) call associated with aggressive interactions. Responsiveness to effective vocal stimuli was reduced or eliminated when the spectrotemporal features of the stimuli were altered in a subset of neurons. Chemical activation of the medial geniculate body (MG) increased both background and evoked firing. Among 39 histologically localized recording sites, we saw no evidence of topographic organization in terms of temporal response pattern, habituation, or the affect of calls to which neurons responded. Overall, these studies demonstrate that amygdalar neurons in the mustached bat show high selectivity to vocal stimuli, and suggest that persistent firing may be an important feature of amygdalar responses to social vocalizations.

A New Spirurid (Nematoda) Parasite from Mormoopid Bats in Mexico

A new nematode species, Spirura mexicana n. sp., is described from specimens recovered from the esophageal mucosa of the Parnell's mustached bat Pteronotus parnellii , Davy's naked-backed bat Pteronotus davyi, Wagner's mustached bat Pteronotus personatus, and the ghost-faced bat Mormoops megalophylla in the State of Morelos, Mexico. This nematode is characterized by having a relatively short prostoma, 5-6 pairs of caudal papillae, and a smooth distal end of the tail in females. This is the first species of Spirura described from bats in the New World.

Properties of echo delay-tuning receptive fields in the inferior colliculus of the mustached bat

One role of the inferior colliculus (IC) in bats is to create neuronal delay-tuning, which is used for the estimation of target distance in the echolocating bat’s auditory system. In this study, we describe response properties of IC delay-tuned neurons of the mustached bat (Pteronotus parnellii) and compare it with those of delay-tuned neurons of the auditory cortex (AC). We also address the question if frequency content of the stimulus (pure-tone (PT) or frequency-modulated (FM) pairs stimulation) affects combination-sensitive interaction in the same neuron. Sharpness and sensitivity of delay-tuned neurons in the IC are similar to those described in the AC. However, in contrast to cortical responses, in collicular neurons the delay at which the neurons show the maximum response does not change with changes in echo level. This tolerance to changes in the echo level seems to be a property of collicular delay-tuned neurons, which is modified along the ascending auditory pathway. In the IC we found neurons that showed a facilitated delay-tuned response when stimulated with FM components and did not show any delay-tuning with PT stimulation. This result suggests that not only is echo delay-tuning generated in the IC but also its FM-specificity observed in the cortex could be created to some extent in the IC and then topographically organized at higher levels.

Simple Syllabic Calls Accompany Discrete Behavior Patterns in CaptivePteronotus parnellii: An Illustration of the Motivation-Structure Hypothesis

Mustached bats, Pteronotus parnellii, are highly social and vocal. Individuals of this species roost in tight clusters, and emit an acoustically rich repertoire of calls whose behavioral significance is largely unknown. We recorded their social and vocal behaviors within a colony housed under semi-natural conditions. We also quantified the spatial spread of each bat's roosting location and discovered that this was relatively fixed and roughly confined to an individual's body width. The spatial precision in roosting was accompanied by an equally remarkable match between specific vocalizations and well-timed, discrete, identifiable postures/behaviors, as revealed by logistic regression analysis. The bodily behaviors included crouching, marking, yawning, nipping, flicking, fighting, kissing, inspecting, and fly-bys. Two echolocation-like calls were used to maintain spacing in the colony, two noisy broadband calls were emitted during fights, two tonal calls conveyed fear, and another tonal call signaled appeasement. Overall, the results establish that mustached bats exhibit complex social interactions common to other social mammals. The correspondence of relatively low frequency and noisy, broadband calls with aggression, and of tonal, high frequency calls with fear supports Morton's Motivation-Structure hypothesis, and establishes a link between motivation and the acoustic structure of social calls emitted by mustached bats.

Social Calls Exhibit a Distributed Consensus Map in the Auditory Cortex of Mustached Bats

Social Calls Exhibit a Distributed Consensus Map in the Auditory Cortex of Mustached Bats

Neural Coding of Call Pitch and Syllable Type in the Auditory Cortex of Mustached Bats

Neural Coding of Call Pitch and Syllable Type in the Auditory Cortex of Mustached Bats

Right–left asymmetry in the cortical processing of sounds for social communication vs. navigation in mustached bats

In the Doppler-shifted constant frequency processing area in the primary auditory cortex of mustached bats, Pteronotus parnellii, neurons respond to both social calls and to echolocation signals. This multifunctional nature of cortical neurons creates a paradox for simultaneous processing of two behaviorally distinct categories of sound. To test the possibility of a stimulus-specific hemispheric bias, single-unit responses were obtained to both types of sounds, calls and pulse-echo tone pairs, from the right and left auditory cortex. Neurons on the left exhibited only slightly higher peak response magnitudes for their respective best calls, but they showed a significantly higher sensitivity (lower response thresholds) to calls than neurons on the right. On average, call-to-tone response ratios were significantly higher for neurons on the left than for those on the right. Neurons on the right responded significantly more strongly to pulse-echo tone pairs than those on the left. Overall, neurons in males responded to pulse-echo tone pairs with a much higher spike count compared to females, but this difference was less pronounced for calls. Multidimensional scaling of call responses yielded a segregated representation of call types only on the left. These data establish for the first time, a behaviorally directed right-left asymmetry at the level of single cortical neurons. It is proposed that a lateralized cortex emerges from multiparametric integration (e.g. combination-sensitivity) within a neuron and inhibitory interactions between neurons that come into play during the processing of complex sounds.

Análisis de la colección de murciélagos (Mammalia: Chiroptera) del Museo Nacional de Historia Natural de Santo Domingo

Se hace la descripción de la colección de murciélagos del Museo Nacional de Historia Natural de Santo Domingo. Se atiende a la composición de la colección y la distribución geográfica de sus especímenes; se hace una actualización taxonómica. Se examinaron 723 especímenes, pertenecientes a seis (6) familias, 17 géneros y 18 especies, estando representadas todas las especies reportadas para La Hispaniola. Todos los géneros son monoespecíficos, con excepción de Pteronotus Gray, 1838 con dos especies. Las fechas de colecta datan desde 1961 y se extienden hasta el 2008, correspondiendo la mayor parte de registros a la Región Suroeste de la República Dominicana. Las especies más abundantes en la colección resultaron ser generalistas en cuanto a selección de refugios, tales como los filostómidos Artibeus jamaicensis y Macrotus waterhousii y el molósido Molossus molossus. Cabe destacar la presencia de especies de cuevas calientes (Pteronotus parnellii, P. quadridens, y Phyllonycteris poeyi), así como especies raras: Chilonatalus micropus, Lasiurus minor y Natalus major.

Prestin Shows Divergent Evolution Between Constant Frequency Echolocating Bats

The gene Prestin encodes a motor protein that is thought to confer the high-frequency sensitivity and selectivity that characterizes the mammalian auditory system. Recent research shows that the Prestin gene has undergone a burst of positive selection on the ancestral branch of the Old World horseshoe and leaf-nosed bats (Rhinolophidae and Hipposideridae, respectively), and also on the branch leading to echolocating cetaceans. Moreover, these two groups share a large number of convergent amino acid sequence replacements. Horseshoe and leaf-nosed bats exhibit narrowband echolocation, in which the emitted calls are based on the second harmonic of a predominantly constant frequency (CF) component, the frequency of which is also over-represented in the cochlea. This highly specialized form of echolocation has also evolved independently in the neotropical Parnell's mustached bat (Pteronotus parnellii). To test whether the convergent evolution of CF echolocation between lineages has arisen from common changes in the Prestin gene, we sequenced the Prestin coding region (~2,212bp, >99% coverage) in P. parnellii and several related species that use broadband echolocation calls. Our reconstructed Prestin gene tree and amino acid tree showed that P. parnellii did not group together with Old World horseshoe and leaf-nosed bats, but rather clustered within its true sister species. Comparisons of sequences confirmed that P. parnellii shared most amino acid changes with its congeners, and we found no evidence of positive selection in the branch leading to the genus of Pteronotus. Our result suggests that the adaptive changes seen in Prestin in horseshoe and leaf-nosed bats are not necessary for CF echolocation in P. parnellii.