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[Model of the system for stabilizing the frequency of the echosignal of the Rhinolophus locator].

Physical analysis of anatomic, physiological and behavioural data pertaining to the work of Rhinolophidae echolocator is carried out, results of spectral analysis of its probing impulse are analysed. On this basis the working mechanism of sound emitting apparatus is proposed. A phenomenological model of the frequency stabilization system of the signal reflected from a located object is constructed. This stabilization is carried out by the compensation of Doppler shift of the echo frequency by a change of the generated impulse frequency. Due to the application of a differential method the model provides for potential accuracy of tuning, and its work does not depend on the value of a reflected signal and its sufficiently small changes which is in agreement with the experiments.

Animals↗

Does the visual system of the flying fox resemble that of primates? The distribution of calcium-binding proteins in the primary visual pathway of Pteropus poliocephalus.

It has been proposed that flying foxes and echolocating bats evolved independently from early mammalian ancestors in such a way that flying foxes form one of the suborders most closely related to primates. A major piece of evidence offered in support of a flying fox-primate link is the highly developed visual system of flying foxes, which is theorized to be primate-like in several different ways. Because the calcium-binding proteins parvalbumin (PV) and calbindin (CB) show distinct and consistent distributions in the primate visual system, the distribution of these same proteins was examined in the flying fox (Pteropus poliocephalus) visual system. Standard immunocytochemical techniques reveal that PV labeling within the lateral geniculate nucleus (LGN) of the flying fox is sparse, with clearly labeled cells located only within layer 1, adjacent to the optic tract. CB labeling in the LGN is profuse, with cells labeled in all layers throughout the nucleus. Double labeling reveals that all PV+ cells also contain CB, and that these cells are among the largest in the LGN. In primary visual cortex (V1) PV and CB label different classes of non-pyramidal neurons. PV+ cells are found in all cortical layers, although labeled cells are found only rarely in layer I. CB+ cells are found primarily in layers II and III. The density of PV+ neuropil correlates with the density of cytochrome oxidase staining; however, no CO+ or PV+ or CB+ patches or blobs are found in V1. These results show that the distribution of calcium-binding proteins in the flying fox LGN is unlike that found in primates, in which antibodies for PV and CB label specific separate populations of relay cells that exist in different layers. Indeed, the pattern of calcium-binding protein distribution in the flying fox LGN is different from that reported in any other terrestrial mammal. Within V1 no PV+ patches, CO blobs, or patchy distribution of CB+ neuropil that might reveal interblobs characteristic of primate V1 are found; however, PV and CB are found in separate populations of non-pyramidal neurons. The types of V1 cells labeled with antibodies to PV and CB in all mammals examined including the flying fox suggest that the similarities in the cellular distribution of these proteins in cortex reflect the fact that this feature is common to all mammals.

Animals↗

Position of the larynx in odontoceti (toothed whales).

This study examines the positional relationships of the odontocete (toothed whale) larynx to further an understanding of their breathing, swallowing, and vocalizing abilities. Seventeen specimens representing nine cetacean genera (Delphinus, Stenella, Tursiops, Grampus, Delphinapterus, Globicephala, Kogia, Mesoplodon, and Phocoena) were studied post mortem. Nine specimens were sectioned in the midsagittal plane and the position of the larynx relative to vertebral levels, skull base, and palatal structures was recorded. In eight specimens that could not be bisected for reasons of large size or condition of preservation, the larynx was removed by a ventral approach for further dissection. The results show that the upper respiratory tract of the odontocetes has evolved away from a basic mammalian pattern. Laryngeal position among terrestrial mammals usually corresponds to the level of cervical vertebrae 1-3. The odontocete larynx, however, lies rostral to the level of the atlas and extends to the presphenoidal synchondrosis. Its extension above the level of the foramen magnum is due to three factors: 1) The larynx is elongated into a tubular extension that projects beyond the soft palate into the nasopharynx; 2) the neck region is shortened owing to the highly compressed cervical vertebrae; and 3) the skull base is oriented in the same direction as the cervical vertebrae because of the horizontal and fusiform alignment of the head and thorax. Whereas the larynx of most terrestrial mammals is separable from the nasopharynx, that of the odontocetes studied may be permanently intranarial, held in place by the palatopharyngeal sphincter. Laryngeal position may affect their vocal abilities, allowing odontocetes to simultaneously swallow and echolocate.

Animals↗

Cortical complexity in cetacean brains.

Cetaceans (dolphins, whales, and porpoises) have a long, dramatically divergent evolutionary history compared with terrestrial mammals. Throughout their 55-60 million years of evolution, cetaceans acquired a compelling set of characteristics that include echolocation ability (in odontocetes), complex auditory and communicative capacities, and complex social organization. Moreover, although cetaceans have not shared a common ancestor with primates for over 90 million years, they possess a set of cognitive attributes that are strikingly convergent with those of many primates, including great apes and humans. In contrast, cetaceans have evolved a highly unusual combination of neurobiological features different from that of primates. As such, cetacean brains offer a critical opportunity to address questions about how complex behavior can be based on very different neuroanatomical and neurobiological evolutionary products. Cetacean brains and primate brains are arguably most meaningfully conceived as alternative evolutionary routes to neurobiological and cognitive complexity. In this article, we summarize data on brain size and hemisphere surface configuration in several cetacean species and present an overview of the cytoarchitectural complexity of the cerebral cortex of the bottlenose dolphin.

Animals↗

Central projections of auditory receptor neurons of crickets.

We describe the central projections of physiologically characterized auditory receptor neurons of crickets as revealed by confocal microscopy. Receptors tuned to ultrasonic frequencies (similar to those produced by echolocating, insectivorous bats), to a mid-range of frequencies, and a subset of those tuned to low, cricket-like frequencies have similar projections, terminating medially within the auditory neuropile. Quantitative analysis shows that despite the general similarity of these projections they are tonotopic, with receptors tuned to lower frequencies terminating more medially. Another subset of cricket-song-tuned receptors projects more laterally and posteriorly than the other types. Double-fills of receptors and identified interneurons show that the three medially projecting receptor types are anatomically well positioned to provide monosynaptic input to interneurons that relay auditory information to the brain and to interneurons that modify this ascending information. The more laterally and posteriorly branching receptor type may not interact directly with this ascending pathway, but is well positioned to provide direct input to an interneuron that carries auditory information to more posterior ganglia. These results suggest that information about cricket song is segregated into functionally different pathways as early as the level of receptor neurons. Ultrasound-tuned and mid-frequency tuned receptors have approximately twice as many varicosities, which are sites of transmitter release, per receptor as either anatomical type of cricket-song-tuned receptor. This may compensate in part for the numerical under-representation of these receptor types.

Animals↗

Topology of the central nucleus of the mustache bat's inferior colliculus: correlation of single unit properties and neuronal architecture.

The central nucleus of the mustache bat's inferior colliculus was studied in Golgi, Nissl, and fiber stained preparations; the neuronal organization and cytoarchitecture were correlated with the tonotopic maps revealed by single cell recordings. Three divisions of the central nucleus were defined by anatomical and physiological criteria: the anterolateral, medial, and dorsoposterior divisions. In horizontal sections, the anterolateral division has pronounced, semicircular fibrodendritic laminae. The dendritic fields of adjacent neurons form rostro-caudally-oriented laminae related to the tonotopic sequence. The neurons in the medial division are similar in size and arrangement, but here the laminar orientation follows the lateral-to-medial axis, with less curvature. The dorsoposterior division has many small disc-shaped and stellate neurons and a different, somewhat less fully expressed, laminar orientation. Each division has a unique frequency representation and tonotopic organization which conform to the pattern of dendritic orientation. In the anterolateral division, frequencies from about 10 kHz to about 59 kHz are represented, whereas the frequency representation in the medial division ranges from about 65 kHz to 110 kHz, and higher. The dorsoposterior division has an isofrequency organization in which the best frequency is characteristic for each bat, ranging from 60 to 64 kHz and varying by only +/- 300 Hz. This frequency corresponds to the dominant echo frequency of the bat's echolocation signals. We suggest that the dorsoposterior division is a hypertrophied isofrequency lamina, with many neurocytological features comparable to the isofrequency laminae in the central nucleus of other mammals.

Animals↗

Origin of ascending projections to an isofrequency region of the mustache bat's inferior colliculus.

The inferior colliculus of the mustache bat is similar in most respects to the inferior colliculus of more commonly studied mammals, but one isofrequency contour, the dorsoposterior division, is greatly overrepresented. The present study utilizes this specialization of the auditory system in the mustache bat to determine the total set of ascending projections to a single isofrequency contour of the inferior colliculus. Within the dorsoposterior division, neurons are all very narrowly tuned to 60 kHz, the major component of this bat's echolocation call. The afferent projections to this isofrequency contour were identified by making deposits of horseradish peroxidase (HRP) within the dorsoposterior division after physiologically defining its borders. Two other frequency representations are present in the central nucleus of the inferior colliculus of the mustache bat, the anterolateral division in which there is an orderly progression of frequencies from 59 down to 20 kHz, and the medial division in which frequencies from 63-120 kHz are represented. In additional experiments, the afferent projections to the medial and anterolateral divisions were examined, providing an anatomical description of the tonotopicity of the lower auditory nuclei. Deposits of HRP in the DPD labeled cells in each of the lower brainstem auditory nuclei that have previously been shown to project to the entire central nucleus of the inferior colliculus. The ascending projections to the dorsoposterior division include contralateral projections from the cochlear nucleus and inferior colliculus, ipsilateral projections from the medial superior olive, ventral and intermediate nuclei of the lateral lemniscus, and bilateral projections from the lateral superior olive and dorsal nucleus of the lateral lemniscus. In most of the nuclei, labeled cells were confined to specific portions of the nuclei, often forming "slabs" of labeled cells across the rostrocaudal extent of most nuclei. These slabs presumably represent the 60 kHz representation in each of the lower nuclei. When deposits of HRP were made into other frequency band representations of the inferior colliculus, in either the medial or anterolateral division, labeled cells again formed slabs in each lower nucleus. However, the location of the slab varied as a function of the best frequency of neurons at the deposit site, and labeled cells were not present within the 60 kHz representation. These results show the general tonotopy of the mustache bat's brainstem auditory nuclei, and with respect to the dorsoposterior division, clearly reveal the total set of projections to a single isofrequency region.(ABSTRACT TRUNCATED AT 400 WORDS)

Afferent Pathways↗

Connections and frequency representation in the auditory brainstem of the mustache bat, Pteronotus parnellii.

The goals of this study were to describe the cochlear frequency map of the mustache bat, Pteronotus parnellii, and to relate the organization of cochlear primary afferents to that of the second-order projections from the cochlear nucleus to the superior olivary complex. Small deposits of horseradish peroxidase (HRP) were placed in the cochlear nucleus at sites that were physiologically characterized with respect to unit-best frequency. From the deposits, labeled fibers were traced in the retrograde direction to the cochlea and in the anterograde direction to the superior olive. Cochleas from both experimental and control animals were examined with light and electron microscopy. The peripheral axons of spiral ganglion neurons were counted in order to quantify the unusual variation in the innervation density along the cochlear spiral of the mustache bat. Regions of increased innervation density were found at the beginning and end of the basal turn of the cochlea. The highest cochlear innervation density consistently occurred in the upper basal turn. In horseradish peroxidase tracing experiments, this region contained labeled fibers only when HRP deposits were made at sites within the cochlear nucleus with unit-best frequencies around 60 kHz. These findings support the suggestion (Kössl and Vater, '85) that the cochlear sites of increased innervation density are related to the neural and behavioral emphasis that this echolocating bat places upon the analysis of the 60 kHz frequency band. The general arrangement of tonotopic maps within the cochlea, cochlear nucleus, and superior olive was consistent with previous observations in this bat and other mammalian species. At all three levels, there was evidence of a disproportionately large representation of frequencies around 60 kHz, similar to the enlarged representation reported within the inferior colliculus and auditory cortex of the mustache bat. In all cases there was a consistent relation between the size of the HRP deposit and the number and distribution of retrogradely labeled neurons in the cochlea. For most cases there was a similar relation between the size of the deposit and the terminal arborization field of anterogradely labeled fibers in the superior olive. However, in cases with deposits associated with the 60 kHz frequency band, the size of the labeled arborization field was more than twice as large as expected from the size of the deposits and from the extent of labeling in the cochlea. These cases suggest that the representation of frequencies around 60 kHz, already overrepresented in both the cochlea and cochlear nucleus, may be further expanded at the level of the superior olivary complex.

Acoustic Stimulation↗

Ultrastructure of the horseshoe bat's organ of Corti. II. Transmission electron microscopy.

The fine structure of the organ of Corti was investigated in the echolocating horseshoe bat (Rhinolophus rouxi) by transmission electron microscopy. Particular emphasis was placed on the receptor cells and their supporting cells. The receptor cells, inner hair cells (IHC) and outer hair cells (OHC), possess the typical mammalian shape, but OHCs are extremely short (length: 12-15 microns in the basal turn and up to 28-30 microns in the apical turn). The afferent innervation of both types of receptor cells and the efferent innervation of the IHC system conform to the general mammalian scheme; however, confirming earlier reports, an efferent innervation to the OHCs is absent. Throughout the cochlea, IHCs and OHCs possess a single layer of subsurface cisternae. Above the level of the nucleus of the OHCs, the arrangements of the subsurface cisternae and their connection to the lateral cell membrane via pillars are highly regular, whereas in IHCs, the cisternae are of irregular shape and the pillar system is much less distinct. In the basal turn of the cochlea, the attachment sites of the OHCs to the supporting cells possess specialized features: (a) in the reticular lamina, the contact sites of the cuticular plates of OHCs with the outer pillar cells and the Deiters cell phalanges are of exaggerated length, and (b) the cup formation of the Deiters cell body, which houses the bottom of the OHC, has a specialized shape and is packed with electron-dense material and microtubules. The results are discussed in relation to cochlear ultrastructure in other mammals and in the context of active processes in cochlear mechanics.

Afferent Pathways↗

Projections of physiologically defined subdivisions of the inferior colliculus in the mustached bat: targets in the medial geniculate body and extrathalamic nuclei.

This study examined the output of the central nucleus of the inferior colliculus to the medial geniculate body and other parts of the nervous system in the mustached bat (Pteronotus parnellii). Small deposits of anterograde tracers (horseradish peroxidase, [3H]leucine, Phaseolus vulgaris leucoagglutinin, wheat germ agglutinin conjugated to horseradish peroxidase, or biocytin) were made at physiologically defined sites in the central nucleus representing major components of the bat's echolocation signal. The topography, frequency specificity, and axonal morphology of these outputs were studied. The medial geniculate body was a major target of inferior collicular neurons, with three distinct input patterns. The projection to the ventral division was tonotopically organized, but had a relatively sparse contribution from neurons representing frequency modulated components of the biosonar pulse. The second input was to the rostral medial geniculate body, in which projections from inferior collicular neurons representing constant frequency sonar components were separated from those representing frequency modulated components. A third input was to the suprageniculate nucleus, which received strong, topographically arranged projections. Inputs to the dorsal nucleus and medial division were also observed. Extrathalamic regions receiving input included the pontine gray, external nucleus of the inferior colliculus, pericollicular tegmentum, nucleus of the brachium of the inferior colliculus, and pretectum. These central nucleus projections differed in organization and the structure of axon terminals, suggesting different physiological influences on their target nuclei. These results demonstrate that the central nucleus has divergent projections to various sensory and premotor nuclei, besides its well-established projection to the medial geniculate body.

Acoustic Stimulation↗

Origin of ascending projections to the nuclei of the lateral lemniscus in the big brown bat, Eptesicus fuscus.

The nuclei of the lateral lemniscus in the echolocating bat, Eptesicus fuscus, are large and highly differentiated. In each nucleus, different characteristic response properties predominate. To determine whether the dissimilar response properties are due in part to differential ascending input, we examined the retrograde transport from small deposits of horseradish peroxidase (HRP) or HRP conjugated with wheat germ agglutinin (WGA-HRP) in the nuclei of the lateral lemniscus. The intermediate nucleus (INLL) and the two divisions of the ventral nucleus (VNLL) receive almost exclusively monaural input from the anteroventral and posteroventral cochlear nuclei and from the medial nucleus of the trapezoid body. Lesser inputs originate in the lateral nucleus of the trapezoid body and the ventral periolivary area. Although the three monaural nuclei of the lateral lemniscus all receive input from the same set of nuclei, and from the same identified cell types in the cochlear nucleus, there is a difference in the relative proportions of input from these sources. The dorsal nucleus (DNLL) receives input mostly from binaural structures, the lateral and medial superior olives and the contralateral DNLL, with only a minor projection from the cochlear nucleus. The lateral and medial superior olives project bilaterally; the bilateral projection from the medial superior olive is unusual in that it is found in only a few mammalian species. The results show a segregated pattern of binaural projections to DNLL and monaural projections to INLL and VNLL that is consistent with the binaural response properties found in DNLL and the exclusively monaural response properties found in INLL and VNLL. The differences in response properties between monaural nuclei, however, are not due to input from different nuclei or cell types but may be influenced by differing magnitudes of the constituent ascending projections.

Afferent Pathways↗

Mercury vapour lamps interfere with the bat defence of tympanate moths (Operophtera spp.; Geometridae)

Bats often forage near streetlamps, where they catch moths in particular. At least two hypotheses may explain the apparent increase in the availability of moths to bats feeding around streetlamps: (1) the moths become concentrated near the light and therefore more profitable to exploit; and (2) the light interferes with the moths' evasive flight behaviour. We tested the second of these hypotheses by exposing flying male winter moths, Operophtera spp., to bursts of ultrasound (26 kHz, 110 dB sound pressure level) from an electronic source. The light from a 125 W mercury vapour lamp had a quantitative effect on the moths' evasive flight response at close range (within ca 4 m), inhibiting it totally in nearly half (43%, N=125) of the cases. By contrast, moths flying in the surrounding woodland and without interference from the lamp always responded to the sound. Streetlamps of the mercury vapour type (white lamps) thus interfere with the defensive behaviour of moths and presumably increase their vulnerability to echolocating bats. This may have implications for the conservation of both moths and bats. Copyright 1998 The Association for the Study of Animal Behaviour.

Journal Article↗

Noctuid moths show neural and behavioural responses to sounds made by some bat-marking rings.

Coloured rings are often used for marking bats so that specific individuals can be recognized. We noticed that the rings of mouse-eared bats, Myotis myotis and Myotis blythii, in a combination of one plastic-split and one metallic ring on the same forearm, emitted sounds that were largely ultrasonic each time the rings met in flight. We recorded the ring sounds and the echolocation calls produced by the bats, and played them back to neural preparations of lesser yellow underwing moths, Noctua comes, while making extracellular recordings from the moths' A1 auditory receptors. The peak energy of the ring sounds occurred much closer in frequency to the moth's best auditory frequency (the frequency at which the moth has the lowest auditory threshold) than the peak energy of the calls, for both bat species, and the ring sounds were detected at a threshold 5-6 dB peSPL lower than the calls. Moths performed evasive manoeuvres to playbacks of ring sounds more frequently than they did to control (tape noise) sequences. These neural and behavioural responses imply that certain bats should not be marked with two rings on one wing, as this may make the bat more apparent to tympanate insects, and may therefore reduce its foraging success. Copyright 1999 The Association for the Study of Animal Behaviour.

Journal Article↗

Evoked potentials of the auditory cortex of the porpoise, Phocoena phocoena.

Evoked potential (EP) recordings in the auditory cortex of the porpoise, Phocoena phocoena, were used to obtain data characterizing the auditory perception of this dolphin. The frequency threshold curves showed that the lowest EP thresholds were within 120-130 kHz. An additional sensitivity peak was observed between 20 and 30 kHz. The minimal EP threshold to noise burst was 3 X 10(-4) - 10(-3) Pa. The threshold for response to modulations in sound intensity was below 0.5 dB and about 0.1% for frequency modulations. Special attention was paid to the dependence of the auditory cortex EP on the temporal parameters of the acoustic stimuli: sound burst duration, rise time, and repetition rate. The data indicate that the porpoise auditory cortex is adapted to detect ultrasonic, brief, fast rising, and closely spaced sounds like echolocating clicks.

Acoustic Stimulation↗

Phonotaxis in flying crickets. I. Attraction to the calling song and avoidance of bat-like ultrasound are discrete behaviors.

The steering responses of three species of field crickets, Teleogryllus oceanicus, T. commodus, and Gryllus bimaculatus, were characterized during tethered flight using single tone-pulses (rather than model calling song) presented at carrier frequencies from 3-100 kHz. This range of frequencies encompasses the natural songs of crickets (4-20 kHz, Fig. 1) as well as the echolocation cries of insectivorous bats (12-100 kHz). The single-pulse stimulus paradigm was necessary to assess the aversive nature of high carrier frequencies without introducing complications due to the attractive properties of repeated pulse stimuli such as model calling songs. Unlike the natural calling song, single tone-pulses were not attractive and did not elicit positive phonotactic steering even when presented at the calling song carrier frequency (Figs. 2, 3, and 9). In addition to temporal pattern, phonotactic steering was sensitive to carrier frequency as well as sound intensity. Three discrete flight steering behaviors positive phonotaxis, negative phonotaxis and evasion, were elicited by appropriate combinations of frequency, temporal pattern and sound intensity (Fig. 12). Positive phonotactic steering required a model calling song temporal pattern, was tuned to 5 kHz and was restricted to frequencies below 9 kHz. Negative phonotactic steering, similar to the 'early warning' bat-avoidance behavior of moths, was produced by low intensity (55 dB SPL) tone-pulses at frequencies between 12 and 100 kHz (Figs. 2, 3, and 9). In contrast to model calling song, single tone-pulses of high intensity 5-10 kHz elicited negative phonotactic steering; low intensity ultrasound (20-100 kHz) produced only negative phonotactic steering, regardless of pulse repetition pattern. 'Evasive', side-to-side steering, similar to the 'last-chance' bat-evasion behavior of moths was produced in response to high intensity (greater than 90 dB) ultrasound (20-100 kHz). Since the demonstration of negative phonotactic steering did not require the use of a calling song temporal pattern, avoidance of ultrasound cannot be the result of systematic errors in localizing an inherently attractive stimulus when presented at high carrier frequencies. Unlike attraction to model calling song, the ultrasound-mediated steering responses were of short latency (25-35 ms) and were produced in an open loop manner (Fig. 4), both properties of escape behaviors.(ABSTRACT TRUNCATED AT 400 WORDS)

Animal Communication↗

Distinctive medium chain wax esters, triglycerides, and diacyl glyceryl ethers in the head fats of the Pacific beaked whale, Berardius bairdi.

Lipids were extracted from the mandibular fat body (jaw), the fatty forehead (melon), and the dorsal blubber of a Pacific beaked whale (Berardius bairdi) and separated into lipid classes by preparative thin layer chromatogrphy. The head fats were mixtures of wax esters and triglycerides with a very small amount of diacyl glyceryl ether. The blubber fat contained 97% wax ester and 3% triglyceride. Gas liquid chromatography (GLC) of the intac lipid classes indicated an unusually low C26-C30 range for most of the jaw and melon wax esters compared to the more normal C32-C40 molecules found in the blubber. Distinctive lower molecular weight C24-C40 triglycerides occurred in the head fats vs. the usual C44-C58 range in the blubber. Most diacyl glyceryl ethers were in the C35-C46 range, below the molecular weight of hexadecyldipalmitoyl glyceryl ether (C48). GLC of the derived fatty acid methyl esters showed that the lower molecular weight neutral lipids in the head fats were due to high levels of iso-10:0, n-10:0, iso-11:0, iso-12:0, N-12:0, and iso-13:0 acids. The wax ester fatty alcohols and the alkoxy chains of the glyceryl ethers were mostly the C14-C20 chain lengths commonly observed in marine organisms. The distinctive medium chain neutral lipids in the jaw and melon fats of this whale may be related to the postulated acoustical role of these tissues in echolocation.

Adipose Tissue↗

Evasive response to ultrasound by the crepuscular butterfly Manataria maculata.

The crepuscular nymphalid butterfly Manataria maculata was studied in Monteverde cloud forest, Costa Rica, during the dry season reproductive diapause. M. maculata has ears in the form of Vogel's organs located near the base of the forewings. Its behaviour in response to bursts of ultrasonic pulses (26 kHz, 110 dB SPL at 1 m) was condition-dependent. At dusk and dawn the sound consistently elicited evasive responses, similar to those of moths, in flying individuals. In contrast day-roosting individuals always remained motionless although they were alert to other stimuli. The daily movements between day- and night-roosts coincided in time and light intensity with the activity of insectivorous bats. This is the first reported case of ultrasonic hearing connected to evasive flights in a true butterfly (Papilionoidea). It strongly supports the idea that echolocating bats were involved in the evolution of hearing in butterflies.

Animals↗

The eyes of oilbirds (Steatornis caripensis): pushing at the limits of sensitivity.

An extreme example of a low light-level lifestyle among flying birds is provided by the oilbird, Steatornis caripensis (Steatornithidae, Caprimulgiformes). Oilbirds breed and roost in caves, often at sufficient depth that no daylight can penetrate, and forage for fruits at night. Using standard microscopy techniques we investigated the retinal structure of oilbird eyes and used an ophthalmoscopic reflex technique to determine the parameters of these birds' visual fields. The retina is dominated by small rod receptors (diameter 1.3+/-0.2 microm; length 18.6+/-0.6 microm) arranged in a banked structure that is unique among terrestrial vertebrates. This arrangement achieves a photoreceptor density that is the highest so far recorded (approximately 1,000,000 rods mm(-2)) in any vertebrate eye. Cone photoreceptors are, however, present in low numbers. The eye is relatively small (axial length 16.1+/-0.2 mm) with a maximum pupil diameter of 9.0+/-0.0 mm, achieving a light-gathering capacity that is the highest recorded in a bird (f-number approximately 1.07). The binocular field has a maximum width of 38 degrees and extends vertically through 100 degrees with the bill projecting towards the lower periphery; a topography that suggests that vision is not used to control bill position. We propose that oilbird eyes are at one end of the continuum that juxtaposes the conflicting fundamental visual capacities of sensitivity and resolution. Thus, while oilbird visual sensitivity may be close to a maximum, visual resolution must be low. This explains why these birds employ other sensory cues, including olfaction and echolocation, in the control of their behaviour in low-light-level environments.

Animals↗