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Hearing in coruros (Spalacopus cyanus): Special audiogram features of a subterranean rodent
Abstract
Learning curves and behavioural audiograms of subterranean, socially living coruros (Spalacopus cyanus) were obtained using a positive reinforcement conditioning procedure. The individually varying audiograms revealed best hearing at frequencies between 1.25 and 1.6 kHz, which corresponds with the common pattern established in subterranean rodents studied so far. However, the broad hearing range covering frequencies at least between 0.25 and 20 kHz coupled with the high sensitivity (average minimum 7 dB) that is found in coruros are atypical features for audiograms of subterranean rodents, which usually show restricted high-frequency hearing ranges and very poor sensitivity. Hearing at low frequencies (peaks at frequencies <1 kHz), which may be related to sound transmission in underground burrows, and high sensitivity at 1.25/1.6 kHz are discussed in relation to vocalization. In addition to these peaks, a third peak at 8 kHz--probably a plesiomorphic feature of mammals--may be of significance in aboveground communication.
... 3.5 Mya; Upham and Patterson, 2012). Behavioral audiograms and morphological observations on this species indicate well-developed hearing, similar in frequency range to that of diverse epigeic small mammals (Begall et al., 2004;Begall and Burda, 2006). In contrast, Pyott et al. (2020) presented evidence for a moderate accumulation of deleterious mutations in the octodontid stem lineage (however, no coruro sequence data were analyzed). ...
... For each study species, we tested 15 different frequencies, which were preselected based on the hearing range determined by available studies on the respective species or congeneric relatives [naked mole rats: 0.03-12 kHz (16 kHz) (Heffner and Heffner, 1993;Okanoya et al., 2018), Mashona mole-rats: 0.03-16 kHz (Gerhardt et al., 2017), coruros: 0.03-32 kHz (36 kHz) (Begall et al., 2004); Table 2]. It became clear during the experiments that coruros exhibit good hearing at 32 kHz, so for three animals an additional 36 kHz step was included (noted in Table 1). ...
... The coruro differed from the two bathyergid species in displaying both a higher sensitivity, with mean thresholds below 20 dB SPL in the region of best hearing, and a far wider auditory range that reaches well into the ultrasonic domain. The ABR results for coruros are in good agreement with previously published behavioral audiograms (Begall et al., 2004). However, responses to frequencies above 20 kHz had not been tested in this species so far. ...
Hearing in subterranean rodents exhibits numerous peculiarities, including low sensitivity and restriction to a narrow range of comparatively low frequencies. Past studies provided two conflicting hypotheses explaining how these derived traits evolved: structural degeneration and adaptive specialization. To further elucidate this issue, we recorded auditory brainstem responses from three species of social subterranean rodents that differ in the degree of specialization to the underground habitat: The naked mole-rat (Heterocephalus glaber) and the Mashona mole-rat (Fukomys darlingi) which represent the ancient lineage of African mole-rats (Bathyergidae) and the coruro (Spalacopus cyanus), a South American rodent (Octodontidae) which adopted a subterranean lifestyle in more recent geological time. Additionally, we measured call amplitudes of social vocalizations to study auditory vocal coupling. We found elevated auditory thresholds and severe low-frequency hearing range restrictions in the African mole-rats, with hearing in naked mole-rats tending to be more sensitive than in Mashona mole-rats. In contrast to that, hearing in coruros was similar to that of epigeic rodents, with its range extending into ultrasonic frequencies. However, as in the mole-rats, the coruros’ region of best hearing was located at low frequencies close to 1 kHz. We argue that the auditory sensitivity of African mole-rats, although remarkably poor, has been underestimated by recent studies, while data on coruros conform to previous results. Considering the available evidence, we propose to be open to both degenerative and adaptive interpretations of hearing physiology in subterranean mammals, as each may provide convincing explanations for specific auditory traits observed.
... Several studies have addressed the hearing capabilities of subterranean and fossorial mammals of different genera (Begall et al., 2004Brückmann and Burda, 1997;Heffner and Heffner, 1990, 1993reviewed in Begall et al., 2017). In comparison to similar-sized epigeic mammals, audiograms of subterranean mammals are characterized by lower frequencies of most-sensitive hearing and extremely restricted high-frequency hearing. ...
... Different symbols represent different individuals. (D) The three audiograms in comparison to those of other rodents demonstrate the restricted frequency range and low absolute sensitivity (adapted fromBegall et al., 2004). Different symbols show the average values of two measurements of the different individuals; the black line represents the average hearing threshold of a species. ...
... Different symbols show the average values of two measurements of the different individuals; the black line represents the average hearing threshold of a species. Audiogram data for coruro fromBegall et al. (2004), laboratory rat fromHeffner et al. (1994a), prairie dog fromHeffner et al. (1994b). ...
... Several studies have addressed the hearing capabilities of subterranean and fossorial mammals of different genera (Begall et al., 2004Brückmann and Burda, 1997;Heffner and Heffner, 1990, 1993reviewed in Begall et al., 2017). In comparison to similar-sized epigeic mammals, audiograms of subterranean mammals are characterized by lower frequencies of most-sensitive hearing and extremely restricted high-frequency hearing. ...
... The morphology of the mole-rat auditory periphery has been well studied (e.g. Lange The three audiograms in comparison to those of other rodents demonstrate the restricted frequency range and low absolute sensitivity (adapted from Begall et al., 2004). Different symbols show the average values of two measurements of the different individuals; the black line represents the average hearing threshold of a species. ...
... Different symbols show the average values of two measurements of the different individuals; the black line represents the average hearing threshold of a species. Audiogram data for coruro from Begall et al. (2004), laboratory rat from Heffner et al. (1994a), prairie dog from Heffner et al. (1994b). ...
Life underground has shaped the auditory sense of subterranean mammals, shifting their hearing range to low frequencies. Mole-rats of the genus Fukomys have, however, been suggested to hear up to 18.5 kHz, unusually high for a subterranean rodent. We present audiograms of three mole-rat species, Fukomys anselli, Fukomys micklemi and the giant mole-rat Fukomys mechowii, based on evoked auditory brainstem potentials. All species showed low sensitivity and restricted hearing ranges at 60 dB SPL extending from 125 Hz to 4 kHz (5 octaves) with most sensitive hearing between 0.8 kHz and 1.4 kHz. The high frequency cut-offs are the lowest found in mammals to date. In contrast to predictions from middle ear morphology, F. mechowii did not show higher sensitivity in the low frequency range than F. anselli These data suggest that the hearing range of Fukomys mole-rats is highly restricted to low frequencies and similar to other subterranean mammals.
... The so-called cochlear audiogram based on the study of acoustic distortion products from the cochlea was described in Fig. 9.2. Combined behavioural audiograms of subterranean rodents in comparison to more fossorial rodents like the coruro (Spalacopus cyanus, dotted line, Begall et al. 2004) and the prairie dog (Cynomys sp., dashed line, . The bold solid line illustrates the audiogram of the laboratory rat as an example of a hearing generalist. ...
... The bold solid line illustrates the audiogram of the laboratory rat as an example of a hearing generalist. The shaded area indicates the minimum and maximum threshold values (dB SPL) at different frequencies for strictly subterranean rodents Heffner RS and Heffner 1990, 1992, 1993Kössl et al. 1996;Brückmann and Burda 1997;Begall et al. 2004). The simple horizontal line shows the 60 dB SPL level of hearing. ...
... The simple horizontal line shows the 60 dB SPL level of hearing. Redrawn from Begall et al. (2004) F. anselli (Kössl et al. 1996). Behavioural audiograms are available for several species of subterranean mammals: Geomys bursarius (Heffner RS and Heffner 1990), Spalax ehrenbergi (Heffner RS and Heffner 1992), Heterocephalus glaber (Heffner RS and Heffner 1993), Fukomys anselli (Brückmann and Burda 1997), Spalacopus cyanus (Begall et al. 2004), and Heliophobius argenteocinereus (Knotková et al. 2005) (cf. ...
In the darkness of the subterranean ecotope, hearing seems to be predestined to counterbalance the visual restrictions similar to the situation familiar in cave dwellers like bats. It is therefore generally assumed that audition and acoustic signals play a major role in communication and alertness of subterranean mammals, and it is not surprising that studies on sensory ecology of subterranean species are biased toward hearing and vocalisations.
... In this work we estimate its length based on the length of the bony cochlear canal, whereas Schleich et al. (2006) measured it directly from basilar membranes themselves. Long basilar membranes in Abrocoma and Ctenomys would enhance the audition in arid environments and in the burrows where low-frequency sounds are better transmitted (Heth et al., 1986;Schleich and Vassallo, 2003;Begall et al., 2004;Scheich and Busch, 2004;Begall and Burda, 2006;Lange et al., 2007). We conclude that at least by the early Miocene caviomorphs exhibit a cochlea in the process of adapting to low-frequency sound sensitivity, because Prospaniomys has a longer cochlea (2.5-3 turns) than several mammals (Ekdale, 2013:table 2), but shorter than the extant studied octodontoids. ...
... It remains to be elucidated why octodontoids, and for sure also caviomorph rodents, evolved adaptations to hearing low-frequency sounds (e.g., long and coiled cochlea, enlarged auditory bullae, and absence of stapedius muscle) early in their evolutionary history. The first issue has been well studied in fossorial rodents in which this character convergently evolved in several groups (Heth et al., 1986;Begall et al., 2004;Lange et al., 2007). But their implications in caviomorphs are still unknown. ...
Caviomorphs, the ctenohystrican rodents endemic to the Neotropics, have a long evolutionary history during the Cenozoic, and is one of the more abundant mammalian groups with striking morphological disparity. Several living taxa have auditory regions adapted to hearing low-frequency sounds, yet almost nothing is known about the basicranium in fossil taxa. The octodontoid Prospaniomys priscus from the lower Miocene of Patagonia, Argentina, exhibits a skull with a curious combination of generalized dental characters and supposed derived tympanic cavity. Owing to the basal phylogenetic position of P. priscus, the study of its basicranium based on high resolution X-ray computed tomography represents an excellent opportunity to study an ancestral morphological pattern. Comparisons with living octodontoids permit the evaluation of the auditory region in an evolutionary context. Our results identified that at least since the early Miocene octodontoids, and certainly caviomorphs, have specializations to enhance low-frequency hearing: highly coiled cochlea, small secondary bony laminae, well-developed tympanic cavity, and reduced or absent stapedius muscle, characters that seem not to be directly related to the environment. Possible generalized or specialized states for the latter features are discussed. The significance of this work lies in the fact that it is the first detailed anatomical description of the auditory regions of a fossil caviomorph, providing a new framework with regards to this region of the skull. SUPPLEMENTAL DATA-Supplemental materials are available for this article for free at www.tandfonline.com/UJVP Citation for this article: Arnaudo, M. E., M. Arnal, and E. G. Ekdale 2020. The auditory region of a caviomorph rodent (Hystricognathi) from the early Miocene of Patagonia (South America) and evolutionary considerations. Journal of Vertebrate Paleontology.
... In this work we estimate its length based on the length of the bony cochlear canal, whereas Schleich et al. (2006) measured it directly from basilar membranes themselves. Long basilar membranes in Abrocoma and Ctenomys would enhance the audition in arid environments and in the burrows where low-frequency sounds are better transmitted (Heth et al., 1986;Schleich and Vassallo, 2003;Begall et al., 2004;Scheich and Busch, 2004;Begall and Burda, 2006;Lange et al., 2007). We conclude that at least by the early Miocene caviomorphs exhibit a cochlea in the process of adapting to low-frequency sound sensitivity, because Prospaniomys has a longer cochlea (2.5-3 turns) than several mammals (Ekdale, 2013:table 2), but shorter than the extant studied octodontoids. ...
... It remains to be elucidated why octodontoids, and for sure also caviomorph rodents, evolved adaptations to hearing low-frequency sounds (e.g., long and coiled cochlea, enlarged auditory bullae, and absence of stapedius muscle) early in their evolutionary history. The first issue has been well studied in fossorial rodents in which this character convergently evolved in several groups (Heth et al., 1986;Begall et al., 2004;Lange et al., 2007). But their implications in caviomorphs are still unknown. ...
Caviomorphs, the ctenohystrican rodents endemic to the Neotropics, have a long evolutionary history during the Cenozoic, and is one of the more abundant mammalian groups with striking morphological disparity. Several living taxa have auditory regions adapted to hearing low-frequency sounds, yet almost nothing is known about the basicranium in fossil taxa. The octodontoid Prospaniomys priscus from the lower Miocene of Patagonia, Argentina, exhibits a skull with a curious combination of generalized dental characters and supposed derived tympanic cavity. Owing to the basal phylogenetic position of P. priscus, the study of its basicranium based on high resolution X-ray computed tomography represents an excellent opportunity to study an ancestral morphological pattern. Comparisons with living octodontoids permit the evaluation of the auditory region in an evolutionary context. Our results identified that at least since the early Miocene octodontoids, and certainly caviomorphs, have specializations to enhance low-frequency hearing: highly coiled cochlea, small secondary bony laminae, well-developed tympanic cavity, and reduced or absent stapedius muscle, characters that seem not to be directly related to the environment. Possible generalized or specialized states for the latter features are discussed. The significance of this work lies in the fact that it is the first detailed anatomical description of the auditory regions of a fossil caviomorph, providing a new framework with regards to this region of the skull. SUPPLEMENTAL DATA-Supplemental materials are available for this article for free at www.tandfonline.com/UJVP Citation for this article: Arnaudo, M. E., M. Arnal, and E. G. Ekdale 2020. The auditory region of a caviomorph rodent (Hystricognathi) from the early Miocene of Patagonia (South America) and evolutionary considerations. Journal of Vertebrate Paleontology.
... It appears to be a general feature of subterranean rodents. The somewhat wider hearing range of the coruro Spalacopus, a fossorial caviomorph, is thought to relate to an increased amount of above-ground behaviour [16]. ...
... The fact that underground tunnels represent a 'low-frequency' environment has been used to explain why vocalizations of subterranean rodents tend to emphasize such frequencies [6,[16][17][18][19]. This suggests that the peripheral auditory systems of these animals might show convergently-derived, low-frequency adaptations, and many similarities have indeed been found between the ear structures of distantly-related groups. ...
Although increasingly popular as a laboratory species, very little is known about the peripheral auditory system of the naked mole-rat, . In this study, middle and inner ears of naked mole-rats of a range of ages were examined using micro-computed tomography and dissection. The ears of five other bathyergid species (, , , and ) were examined for comparative purposes. The middle ears of bathyergids show features commonly found in other members of the Ctenohystrica rodent clade, including a fused malleus and incus, a synovial stapedio-vestibular articulation and the loss of the stapedius muscle. deviates morphologically from the other bathyergids examined in that it has a more complex mastoid cavity structure, poorly-ossified processes of the malleus and incus, a 'columelliform' stapes and fewer cochlear turns. Bathyergids have semicircular canals with unusually wide diameters relative to their radii of curvature. How the lateral semicircular canal reaches the vestibule differs between species. has much more limited high-frequency hearing than would be predicted from its small ear structures. The spongy bone forming its ossicular processes, the weak incudo-stapedial articulation, the columelliform stapes and (compared to other bathyergids) reduced cochlear coiling are all potentially degenerate features which might reflect a lack of selective pressure on its peripheral auditory system. Substantial intraspecific differences were found in certain middle and inner ear structures, which might also result from relaxed selective pressures. However, such interpretations must be treated with caution in the absence of experimental evidence.
... It appears to be a general feature of subterranean rodents. The somewhat wider hearing range of the coruro Spalacopus, a fossorial caviomorph, is thought to relate to an increased amount of above-ground behaviour [16]. ...
... The fact that underground tunnels represent a 'low-frequency' environment has been used to explain why vocalizations of subterranean rodents tend to emphasize such frequencies [6,[16][17][18][19]. This suggests that the peripheral auditory systems of these animals might show convergently-derived, low-frequency adaptations, and many similarities have indeed been found between the ear structures of distantly-related groups. ...
Although increasingly popular as a laboratory species, very little is known about the peripheral auditory system of the naked mole-rat, Heterocephalus glaber. In this study, middle and inner ears of naked mole-rats of a range of ages were examined using micro-computed tomography and dissection. The ears of five other bathyergid species (Bathyergus suillus, Cryptomys hottentotus, Fukomys micklemi, Georychus capensis and Heliophobius argenteocinereus) were examined for comparative purposes. The middle ears of bathyergids show features commonly found in other members of the Ctenohystrica rodent clade, including a fused malleus and incus, a synovial stapedio-vestibular articulation and the loss of the stapedius muscle. Heterocephalus deviates morphologically from the other bathyergids examined in that it has a more complex mastoid cavity structure, poorly-ossified processes of the malleus and incus, a ‘columelliform’ stapes and fewer cochlear turns. Bathyergids have semicircular canals with unusually wide diameters relative to their radii of curvature. How the lateral semicircular canal reaches the vestibule differs between species. Heterocephalus has much more limited high-frequency hearing than would be predicted from its small ear structures. The spongy bone forming its ossicular processes, the weak incudo-stapedial articulation, the columelliform stapes and (compared to other bathyergids) reduced cochlear coiling are all potentially degenerate features which might reflect a lack of selective pressure on its peripheral auditory system. Substantial intraspecific differences were found in certain middle and inner ear structures, which might also result from relaxed selective pressures. However, such interpretations must be treated with caution in the absence of experimental evidence.
... In tunnels, airborne sounds of low frequencies are least attenuated (Heth et al. 1986) and even accentuated over short distances (Lange et al. 2007). In subterranean rodents studied thus far, the frequency range of the best hearing is shifted to match the frequencies best propagated in tunnels (Heth et al. 1986;Heffner and Heffner 1990, 1993Müller et al. 1992;Kössl et al. 1996;Brückmann and Burda 1997;Begall et al. 2004). Compared to the epigeic generalized rodents, such as the Norway rat (cf. ...
... Similar to other subterranean rodents, the vocal repertoire of the giant mole-rat consists of several types of tonal and atonal sounds and several mechanical sounds (cf. Pepper et al. 1991;Credner et al. 1997;Francescoli 2000;Veitl et al. 2000;Begall et al. 2004;Schleich et al. 2007). Contact calls of the giant mole-rat include many sequences with nonlinear phenomena like sub-harmonics, deterministic chaos and bifurcation ( Figure 5(c),(d)) which, along with the differences in fundamental frequency, are essential cues for individual recognition (Fitch et al. 2002). ...
... In tunnels, airborne sounds of low frequencies are least attenuated (Heth et al. 1986) and even accentuated over short distances (Lange et al. 2007). In subterranean rodents studied thus far, the frequency range of the best hearing is shifted to match the frequencies best propagated in tunnels (Heth et al. 1986;Heffner and Heffner 1990, 1993Müller et al. 1992;Kössl et al. 1996;Brückmann and Burda 1997;Begall et al. 2004). Compared to the epigeic generalized rodents, such as the Norway rat (cf. ...
... Similar to other subterranean rodents, the vocal repertoire of the giant mole-rat consists of several types of tonal and atonal sounds and several mechanical sounds (cf. Pepper et al. 1991;Credner et al. 1997;Francescoli 2000;Veitl et al. 2000;Begall et al. 2004;Schleich et al. 2007). Contact calls of the giant mole-rat include many sequences with nonlinear phenomena like sub-harmonics, deterministic chaos and bifurcation ( Figure 5(c),(d)) which, along with the differences in fundamental frequency, are essential cues for individual recognition (Fitch et al. 2002). ...
In subterranean ecotope, where absence of light and ventilation limits visual and olfactory communication, options for long-range communication are restricted. Sound is thus one of the few channels available for transfer of the intraspecific information if the animals are not in direct contact. Nevertheless, even this kind of communication is limited by the acoustic conditions of the burrows. It is known that low-frequency sounds are best propagated here. In our study, we describe the vocal repertoire of the social subterranean rodent, the giant mole-rat (Fukomys mechowii, Bathyergidae), from mesic Afrotropics. Its vocal repertoire is shifted to lower frequencies than in other subterranean rodents. The giant mole-rat has the richest vocal repertoire among all subterranean rodents studied so far. In four behavioural contexts, we distinguished 14 single sounds of true vocalization and four types of mechanical communication. Additionally, one seismic (soil-borne) signal of unclear function has been identified. We suggest that the rich vocal repertoire is connected with rich social interactions in giant mole-rat families.
... Airborne sound of a few hundred Hertz has been found to travel best in the subterranean tunnels of the mole-rat Nannospalax ehrenbergi (Heth et al., 1986), and many behavioral and electrophysiological studies have shown that the hearing of fossorial rodents is most sensitive within a low-frequency range Mü ller and Burda, 1989;Heffner and Heffner, 1990, 1992b, 1993Brü ckmann and Burda, 1997;Begall et al., 2004). Certain anatomical features of the ear of fossorial rodents have been interpreted as adaptations mediating lowfrequency hearing (Burda et al., 1988(Burda et al., , 1992Lange et al., 2004;Schleich and Busch, 2004). ...
... Neurotrichus seems to respond behaviorally to frequencies between 8 and 30 kHz (Dalquest and Orcutt, 1942), supporting the prediction that the hearing range of Group 1 talpids extends to higher frequencies than that of Group 2 species. Hearing is known to extend to higher frequencies in burrowing rodents that spend time above ground than in more exclusively subterranean species (Heffner et al., 1994(Heffner et al., , 2001Begall et al., 2004). ...
The middle ear structures of eight species of mole in the family Talpidae (Mammalia: Eulipotyphla) were studied under light and electron microscopy. Neurotrichus, Parascalops, and Condylura have a simple middle ear cavity with a loose ectotympanic bone, ossicles of a "microtype" morphology, and they retain a small tensor tympani muscle. These characteristics are ancestral for talpid moles. Talpa, Scalopus, Scapanus, and Parascaptor species, on the other hand, have a looser articulation between malleus and ectotympanic bone and a reduced or absent orbicular apophysis. These species lack a tensor tympani muscle, possess complete bullae, and extensions of the middle ear cavity pneumatize the surrounding basicranial bones. The two middle ear cavities communicate in Talpa, Scapanus, and Parascaptor species. Parascaptor has a hypertrophied malleus, a feature shared with Scaptochirus but not found in any other talpid genus. Differences in middle ear morphology within members of the Talpidae are correlated with lifestyle. The species with middle ears closer to the ancestral type spend more time above ground, where they will be exposed to high-frequency sound: their middle ears appear suited for transmission of high frequencies. The species with derived middle ear morphologies are more exclusively subterranean. Some of the derived features of their middle ears potentially improve low-frequency hearing, while others may reduce the transmission of bone-conducted noise. By contrast, the unusual middle ear apparatus of Parascaptor, which exhibits striking similarities to that of golden moles, probably augments seismic sensitivity by inertial bone conduction.
... Hearing, ears, and vocalizations are among the most intensely studied topics of sensory ecology in subterranean mammals. Compared to a plethora of papers on anatomy and function of the ear (Begall and Burda 2006;Burda et al. 1989Burda et al. , 1992Kössl et al. 1996;Mason 2001;Müller et al. 1992;Schleich and Busch 2004;Wilkins et al. 1999), hearing (Begall et al. 2004;Brückmann and Burda 1997;Heffner and Heffner 1990, 1993Müller and Burda 1989), and vocalizations (Credner et al. 1997;Heth et al. 1988;Nevo et al. 1987;Pepper et al. 1991;Schleich and Busch 2002;Veitl et al. 2000), however, only one study has dealt with propagation of airborne sounds in burrows (Heth et al. 1986). It showed that in a burrow of the blind mole-rat (Spalax ehrenbergi), sounds were only transmitted over short distances (up to 5 m), and signals of 440 Hz were transmitted better than sounds of lower and higher frequencies; these findings correspond to the frequency characteristics of best hearing and vocalizations in the blind mole-rat. ...
... Vocalizations of several species representing five subterranean rodent genera studied so far (Fukomys, Ctenomys, Heterocephalus, Spalacopus, and Spalax) showed tuning to a lower frequency range than that in above-ground rodents (Credner et al. 1997;Heth et al. 1988;Nevo et al. 1987;Pepper et al. 1991;Schleich and Busch 2002;Veitl et al. 2000). Correspondingly, behavioural audiograms of five species of five subterranean rodent genera (Fukomys, Geomys, Heterocephalus, Spalacopus and Spalax) revealed the highest hearing sensitivity in this lower frequency range (0.5-4 kHz; Begall et al. 2004;Brückmann and Burda 1997;Heffner and Heffner 1990, 1993. These subterranean rodent features are exceptional as the best hearing and vocalizations in similarly sized surfacedwelling rodents are about 8-16 kHz or higher. ...
Subterranean mammals rely to a great extent on audition for communication and to be alerted to danger. The only hitherto published report on burrow acoustics revealed that in tunnels of blind mole-rats (Spalax ehrenbergi), airborne sounds of 440 Hz propagated best whereas lower and higher frequencies were effectively attenuated. Morpho-functional analyses classify the ear of subterranean mammals as a low-sensitivity and low-frequency device. Concordantly, hearing is characterized by low sensitivity and a restricted frequency range tuned to low frequencies (0.5-4 kHz). Some authors considered the restricted hearing in subterranean mammals vestigial and degenerate due to under-stimulation. In contrast to this view stand a rich (mostly low-frequency) vocal repertoire and progressive structural specializations of the middle and inner ear. Thus, other authors considered these hearing characteristics adaptive. To test the hypothesis that acoustical environment in burrows of different species of subterranean mammals is similar, we measured sound attenuation in burrows of Fukomys mole-rats (formerly known as Cryptomys, cf. Kock et al. 2006) of two differently sized species at different locations in Zambia. We show that in these burrows, low-frequency sounds (200-800 Hz) are not only least attenuated but also their amplitude may be amplified like in a stethoscope (up to two times over 1 m). We suggest that hearing sensitivity has decreased during evolution of subterranean mammals to avoid over-stimulation of the ear in their natural environment.
... Compared to aboveground rodents, subterranean habitats are considered more stable and buffered than aboveground habitats. This shelter not only protects these animals from predators, but also from environmental fluctuations or extremes taking place above the ground 6 . However, sometimes, their tunnels are opened inadvertently because of trampling by livestock or researchers using open-hole assessments to monitor their population dynamics 7,8 . ...
... Compared to aboveground rodents, subterranean habitats are considered more stable and buffered than aboveground habitats. This shelter not only protects these animals from predators, but also from environmental fluctuations or extremes taking place above the ground 6 . However, sometimes, their tunnels are opened inadvertently because of trampling by livestock or researchers using open-hole assessments to monitor their population dynamics 7,8 . ...
Defensive behaviors are a response to immediate and potential threats in the environment, including abiotic and biotic threats. Subterranean rodents exhibit morphological and physiological adaptions for life underground, and they will seal with mounds and additional plugs when their burrow opened. However, little is known about the factors driving this defensive behavior. In this study, we selected a subterranean rodent, plateau zokor (Myospalax fontanieri), as a species to investigate (both in the laboratory and in the field) the possible factors responsible for burrow-sealing behavior. Our results showed that: (1) In the laboratory, the burrow-sealing frequency of plateau zokor in response to five factors were as follows: oxygen (52.63%) > light (34.58%) > temperature (20.24%) > gas flow (6.48%) > sound/control (0%). Except for light, the burrow-sealing frequency in response to other factors was significantly lower than that in response to oxygen (P < 0.05). (2) Burrow-sealing behavior in response to each treatment did not differ significantly between males and females in the laboratory experiment. (3) In the field, during the animal’s active periods in both the cold and warm season, the burrow-sealing frequency under the oxygen treatment was higher than that under the light and temperature treatments. Plateau zokors were found not to be sensitive to these treatments during their inactive periods during both the cold and warm season. (4) The latency to reseal the burrow showed no obvious differences between each treatment both in the laboratory and in the field. In conclusion, the main factor that influences the burrow-sealing behavior of plateau zokors is the variation in oxygen concentration, and this defensive behavior is related to their activity rhythm.
... The auditory adaptations of subterranean rodents include the hearing sensitivity shifted to low frequencies compared to the animals of similar size Heffner 1992, 2016;Begall et al. 2004Begall et al. , 2007bGerhardt et al. 2017). Correspondingly, the audible calls produced by subterranean rodents in captivity (Nevo 1979(Nevo , 1990Burda et al. 1990a;Credner et al. 1997;Francescoli 1999;Veitl et al. 2000;Schleich and Busch 2002) are lower in f0 than in surface-dwelling rodents of similar size (Schleich and Francescoli 2018). ...
This study provides the first evidence of ultrasonic vocalisations (USVs) in a truly subterranean rodent, the northern mole vole Ellobius talpinus. Calls were recorded by attracting callers with a bait to burrow entrances, where they were mostly visible to researchers. USVs recorded from 14 different burrows in southern Russia were verified as belonging to Ellobius talpinus by comparison with USVs of two wild-captured young males and by comparison with USVs of four adults from a captive colony. As a first attempt at exploring the function of USV diversity, we defined upward-intense USVs, with a maximum fundamental frequency (f0) of 35.32 ± 5.11 kHz, and variable-faint USVs, with a maximum f0 of 31.40 ± 7.78 kHz. Compared to variable-faint USVs, the upward-intense USVs were longer, had a larger depth of frequency modulation and were produced at high intensity in regular series. The upward-intense USVs were lower in the maximum and peak frequencies in the wild than in captivity, whereas the variable-faint USVs did not differ between recordings from the wild and from captivity. We discuss that similar ranges of acoustic variables found in USVs of Ellobius talpinus and surface-dwelling Arvicolinae species do not support the hypothesis that subterranean life has drastically reduced ultrasonic vocalisation in rodents. ARTICLE HISTORY
... This "subterranean" tuning of hearing can be, on the other hand, disadvantageous during surface activity, because low frequency hearing together with the absence of pinnae impair the localization of sound sources, and thus may increase predation risk (Heffner and Heffner 1990, 1993. On the contrary, fossorial rodents (sensu the above definition) may need more sensitive hearing at higher frequencies and pinnae enabling sound localization (Heffner et al. 1994;Bradbury and Vehrencamp 1998;Begall et al. 2004). We may suppose that sensitive hearing of higher frequencies is also mirrored in ear morphology with the parameters being intermediate between subterranean and epigeic (i.e., active also aboveground) rodents (Lange et al. 2004;Begall and Burda 2006). ...
It is supposed that the subterranean lifestyle in mammals is reflected in ear morphology and tuning of hearing to low frequencies. We studied two root-rat species to see if their ear morphology reflects the difference in the amount of their surface activity. Whereas the more subterranean Tachyoryctes splendens possesses shorter pinnae as expected, it has smaller bullae compared to the more epigeic Tachyoryctes macrocephalus. The ratio between the eardrum and the stapedial footplate area and the ratio between the mallear and the incudal lever were lower in T. splendens (19.3 ± 0.3 and 1.9 ± 0.0, respectively) than in T. macrocephalus (21.8 ± 0.6 and 2.1 ± 0.1), probably reflecting the latter’s higher surface activity. The cochlea in both species has 3.5 coils, yet the basilar membrane is longer in the smaller T. splendens (13.0 ± 0.5 versus 11.4 ± 0.7 mm), which indicates its wider hearing range and/or higher sensitivity (to some frequencies). In both root-rat species, the highest density of outer hair cells (OHC) was in the apical part of the cochlea, while the highest density of inner hair cells (IHC) was in its middle part. This OHC density pattern corresponds with good low-frequency hearing, whereas the IHC pattern suggests sensitivity to higher frequencies.
... On the other hand, it is necessary for the fossorial rodents to hear properly aboveground. Their hearing sensitivity complies with the aboveground conditions and their need to localize the sound source results in preserved high-frequency hearing [19]. ...
Vocal communication is crucial for fossorial and subterranean rodents thanks to the special sensory environment in their underground burrows. The intersection between the research on vocalization and hormones is very small in these rodents. The reproductive hormones seem to influence the tuc-tuc calls in ctenomyids. The naked mole-rat nonbreeders respond to pup calls thanks to the estradiol administered to them by the breeding female through coprophagy. The vocal recognition of reproductive status in Mashona mole-rats is probably independent of their hormonal profile. Oxytocin receptor distribution differs between social and solitary species in both ctenomyids and bathyergids. This review raises more questions than answers, such as how the hormonal levels influence the physical features of the calls in this special acoustic environment or the role of oxytocin in widening the vocal repertoires of social species.
... The level of background noise is high and higher frequencies are attenuated, while lower frequencies in the range of about 200-800 Hz are best propagated (Heth et al., 1986;Lange et al., 2007). Accordingly, the hearing range in subterranean rodents is restricted, and, at the same time, best hearing is shifted to the given low frequency range as demonstrated by behavioral testing (Begall et al., 2004;Brückmann and Burda, 1997;Heffner and Heffner, 1990, 1992, 1993. The properties of tunnel acoustics and hearing are reflected also in vocalization characteristics, which also are tuned to lower frequencies (Bednářová et al., 2013;Credner et al., 1997;Dvořáková et al., 2016;Heth et al., 1986;Knotková et al., 2009;Pepper et al., 1991;Vanden Hole et al., 2014;Veitl et al., 2000). ...
Acoustic conditions in burrows are different from those aboveground and restrict hearing of subterranean mammals to low frequencies, which is reflected in the ear morphology. While low-frequency adaptations of the middle ear attracted more attention of researches, the inner ear remained rather understudied. Here, we examined the cochlea of the inner ear of the Gansu zokor (Eospalax cansus), a subterranean rodent from the Tibetan Plateau. We focused on the quantitative parameters of the organ of Corti, which are assumed to determine hearing sensitivity and frequency tuning. Apart from the morphological traits common to the ear of subterranean rodents studied thus far, the Gansu zokor shows two unique features: the presence of a fourth row of outer hair cells along 20% to 50% of the basilar membrane length and almost constant width of the organ of Corti over more than 10% of its spiral length. Both these anomalies occur in the middle of the cochlear spiral. These features are unusual in comparative morphology of the organ of Corti and presumably are reflected in the functional specialization. They are expected to affect sensitivity and /or resolution of hearing in the frequency range registered in the given cochlear segment. The Gansu zokor thus profiles to an interesting candidate for hearing research which might provide further insight not only into morpho-functional adaptations in subterranean mammals in particular but also in the function of outer hair cells in general.
... Low frequency hearing appears to be a common characteristic of subterranean hearing, and low frequency vocalizations are common for these species as well (Bruns et al. 1988;Burda et al. 1992;Credner et al. 1997;Nevo 1999). This pattern has been reported for the Zambian mole-rat (Africa; Brückmann and Burda 1997;Credner et al. 1997), the blind mole-rat (Europe; Nevo et al. 1987;Heth et al. 1988;Bronchti et al. 1989), and the coruro (South America; Veitl et al. 2000;Begall et al. 2004). ...
Naked mole-rats are extremely social and extremely vocal rodents, displaying a wide range of functionally distinct call types and vocalizing almost continuously. Their vocalizations are low frequency, and a behavioral audiogram has shown that naked mole-rats, like other subterranean mammals, hear only low frequencies. Hence, the frequency range of their hearing and vocalizations appears to be well matched. However, even at low frequencies, naked mole-rats show very poor auditory thresholds, suggesting vocal communication may be effective only over short distances. However, in a tunnel environment where low frequency sounds propagate well and background noise is low, it may be that vocalizations travel considerable distances at suprathreshold intensities. Here, we confirmed hearing sensitivity using the auditory brainstem response; we characterized signature and alarm calls in intensity and frequency domains and we measured the effects of propagation through tubes with the diameter of naked mole-rat tunnels. Signature calls—used for intimate communication—could travel 3–8 m at suprathreshold intensities, and alarm calls (lower frequency and higher intensity), could travel up to 15 m. Despite this species’ poor hearing sensitivity, the naked mole-rat displays a functional, coupled auditory-vocal communication system—a hallmark principle of acoustic communication systems across taxa.
... Such traits can be found in the fossorial tuco-tuco (Ctenomys talarum) and the coruro (Spalacopus cyanus) as well as in surface dwellers such as the guinea pig (Cavia porcellus) or the chinchilla (Chinchilla lanigera;Schleich and Busch, 2004;Begall and Burda, 2006;Argyle and Mason, 2008). Low frequency hearing together with the associated morphological traits was found in many other hystricomorphs irrespective of their style of life (Miller, 1970;Heffner et al., 1971;Begall et al., 2004) suggesting its plesiomorphic state for the hystricomorphs (Begall and Burda, 2006;Argyle and Mason, 2008). There is a higher diversity in hearing specialization within the myomorphs than in hystricomorphs. ...
In spite of the growing interest in rodents with subterranean activity in general and the spalacids (Spalacidae) in particular, little is known about the biology of most members of this clade, such as the Chinese bamboo rat (Rhizomys sinensis). Here, we analyzed the ear morphology of R. sinensis with respect to hearing specialization for subterranean or aboveground modes of communication. It is well-known that ecology and style of life of a particular species can be reflected in morphology of its ear, its hearing and vocalization, so we expect that such information could provide us insight into its style of life and its sensory environment. The ratio between the eardrum and stapedial footplate areas, which influences the efficiency of middle ear sound transmission, suggests low hearing sensitivity, as is typical for subterranean species. The cochlea had 3.25 coils and resembled species with good low frequency hearing typical for subterranean mammals. The length of the basilar membrane was 18.9 ± 0.8 mm and its width slowly increased towards the cochlear apex from 60 to 85 μm. The mean density of outer hair cells was 344 ± 22 and of inner hair cells 114 ± 7.3 per 1 mm length of the organ of Corti, and increased apically. These values (except for relatively low hair cell density) usually characterize ears specialized for low frequency hearing. There was no evidence for an acoustic fovea. Apart of low hair cell density which is common in aboveground animals, this species has also relatively large auricles, suggesting the importance of sound localization during surface activity. The ear of the Chinese bamboo rat thus contains features typical for both aboveground and subterranean mammals and suggests that this spalacid has fossorial habits combined with regular aboveground activity. J. Morphol., 2016. © 2016 Wiley Periodicals, Inc.
... An individual with a sensitive ear living in a noisy environment would be frequently exposed to elevated noise levels which might impact negatively on reproduction and survival, from alteration of normal behavioral activities, chronic stress to permanent loss of hearing in the long run. The 'sensory overstimulation' hypothesis has been put forward, for example, to explain the reduced auditory sensitivity of subterranean rodents in comparison to more fossorial and aboveground rodents (Begall et al., 2004), or the low sensitivity of electroreceptors in African freshwater electric fishes exposed to the more or less continuous electrical noise of lightning storms (Hopkins, 1988). ...
... It has been shown previously that in burrows, sounds of relatively low frequencies (about 0.5 -1 kHz) propagate best (i.e. are least attenuated) and are even enhanced due to the acoustic characteristics of the tunnel systems (Heth et al. 1986;Lange et al. 2007). Consequently, audition is shifted mainly to the low-frequency range (Müller & Burda 1989, Heffner and Heffner 1992, Kössl et al. 1996, Brückmann and Burda 1997, Begall et al. 2004, with the hearing apparatus tuned to these sounds , Müller et al. 1992, and reviewed in Burda 2006. ...
African mole-rats (Bathyergidae) display different levels of sociality, ranging from solitary to eusocial. To integrate individuals into a social group, communication is necessary. In this study, we examined vocalizations of a social bathyergid, Fukomys micklemi, in order to investigate the relationship between sociality and communication. Because of its social organization and subterranean lifestyle, we expected this species to have an extensive vocal repertoire. Fifteen different adult specific call-types and four juvenile specific call-types could be recognized, similar to those in other social species. A new call-category, linked to submissive behaviour, is described. These submissive calls were exclusively observed in males, indicating their subordinance. The vocal repertoire of F. micklemi was compared with published results on vocalizations in other subterranean rodents, both in social and solitary species. This comparison confirmed the observation that the vocal repertoire of social species is not only more extensive, but also more diverse than that of solitary species.
... They were less diversified in comparison to mating calls. Generally, the vocal repertoire of Silvery Mole-rats as a whole is shifted towards lower frequencies compared to aboveground mammals of the same size (Heffner et al. 1971;Heffner et al. 2001), consistent with findings in other subterranean mammals (Pepper et al. 1991;Credner et al. 1997;Francescoli 1999;Veitl et al. 2000;Schleich & Busch 2002;Begall et al. 2004). ...
We examined vocalisations of a solitary subterranean rodent, the Silvery Mole-rat Heliophobius argenteocinereus (Bathyergidae). Seven true vocalisations and one mechanical vocalisation were identified. The main frequencies of the analysed sounds (0.34–13.17 kHz) match to a great extent the frequency range suitable for transmission in underground burrows. Due to the narrow frequency range of vocalisations, motivation is predominantly expressed by the rate of tonality rather than by frequency changes. The vocal repertoire of the Silvery Mole-rat perfectly matches to Morton's MS rules, i.e. that low-frequency and harsh vocalisations indicate hostility whereas high tonal calls signalise appeasement or fear. In comparison with social species, this solitary bathyergid produces fewer calls. It lacks contact and alarm calls, but has a rich repertoire of mating calls (mating ends with duet vocalization of male and female). Acoustic signals seem to play a major role in lowering natural aggressiveness during the mating period.
... Among the species considered in this study, wild Cavia and Chinchilla are usually considered to be nonburrowing (Ebensperger and Blumstein 2006), although Chinchilla may construct small burrows under rocks (Spotorno et al. 2004). Of the octodontoids, Octodon is semifossorial (Ebensperger and Bozinovic 2000), whereas although considered subterranean specialists, Ctenomys species are known to forage above ground, and there is some evidence for aboveground activity in Spalacopus too (Begall et al. 2004;Busch et al. 2000). These genera can loosely be ranked as Spalacopus . ...
By comparison with murine rodents such as rats, the middle ear structures of many subterranean mammals appear to be enlarged and thus adapted toward low-frequency sound transmission. However, comparison with closely related terrestrial outgroups has not always been undertaken, and apparent specializations in some cases might reflect phylogeny rather than habitat. Examination of the middle ear of the nonsubterranean degu (Octodon degus) under light microscopy revealed a septated middle ear cavity, a circular tympanic membrane lacking a pars flaccida, a malleus with elongated head, synostosed with the incus, a typically bicrurate stapes, and no stapedius muscle. Many of these features are shared with closely related, subterranean octodontoids in the genera Ctenomys (tuco-tucos) and Spalacopus (coruro). Caviomorph rodents in general share a very similar middle ear morphology, regardless of habitat, which suggests that sensitive low-frequency hearing is plesiomorphic for this group, rather than being specifically associated with a subterranean lifestyle.
... Moreover, hearing thresholds in the mole-rats studied are higher (i.e., hearing sensitivity is lower) than in their epigeic counterparts (cf., table 1). It should be mentioned at this point that behavioural audiograms of S. ehrenbergi and F. anselli reveal similar characteristics to audiograms of all other subterranean or fossorial rodents studied thus far: Geomys bursarius (Heffner and Heffner, 1990), Heterocephalus glaber (Heffner and Heffner, 1993), Spalacopus cyanus (Begall et al., 2004) and Heliophobius argenteocinereus (Knotkova et al., 2005). ...
The hearing and visual ecology of mole-rats, Spalax ehrenbergi (Spalacidae) from Israel and Fukomys (formerly Cryptomys) anselli (Bathyergidae) from Zambia, two rodent taxa that have independently adapted to subterranean life, are reviewed and compared with epigeic counterparts, the laboratory rat and the guinea pig. In burrows, airborne sounds of low frequencies (200-800 Hz) are least attenuated and even accentuated over short distances. In both mole-rat species the frequency range of the best hearing is shifted to match the frequencies best propagated in tunnels: hearing sensitivity in the lower frequency range (<16 kHz) has been conserved or further improved. Compared to the rat, the hearing range (covering about eight octaves) in mole-rats is not restricted but only shifted towards lower frequencies.Morphologies of the middle and inner ears of mole-rats and the guinea pig are similar in some aspects and suggest tuning to low frequencies. The middle ear morphology of mole-rats does not seem to explain the lower high-frequency limit of hearing. Middle ear is not reduced or degenerated. On the contrary, the incus and the stapedial footplate are markedly enlarged, resulting in reduced sensitivity. These features can be considered an adaptation to compensate for local sound amplification in burrows. The cochlea and its components are highly specialised for sensitive perception and high resolution of low frequencies.Despite living in the same optic environment, Spalax and Fukomys show different degrees of regression and specialisation of the visual system. The eye in Spalax is severely regressed and shortwave-opsin cones are missing. Spalax is blind but the retina has retained its role for photoperiodic perception. Fukomys has small, yet morphologically normal, eyes, with a retina rich in 'blue' cones. It has retained basic visual capabilities; however, the role of light as a zeitgeber is not conclusive.
... Further studies have to elucidate the specific visual needs and behavioral capabilities of the cururo, and indeed of other subterranean mammals. As an interesting parallel, a recent behavioral study indicates that in addition to adaptations to subterranean hearing, cururos have retained some features useful for above-ground hearing and communication (Begall et al., 2004). ...
Subterranean mammals are generally considered to have reduced eyes and apparent blindness as a convergent adaptation to their lightless microhabitat. However, there are substantial interspecific differences. We have studied the prospect of vision in the Chilean subterranean rodent cururo (Spalacopus cyanus, Octodontidae) by analyzing the optical properties of the eye, the presence and distribution of rod and cone photoreceptors, and their spectral sensitivities. Cururo eye size is normal for rodents of similar body size, the cornea and lens are transparent from red to near-UV light, and the retina is well-structured. Electroretinography reveals three spectral mechanisms: a rod with peak sensitivity (lambda(max)) at about 500 nm, a cone with lambda(max) at about 505 nm (green-sensitive L-cone), and a cone with lambda(max) near 365 nm (UV-sensitive S-cone). This suggests dichromatic color vision. Immunocytochemistry with opsin-specific antibodies confirms the presence of rods, L-cones, and S-cones. Cururo rod density is much lower than that of nocturnal surface-dwelling rodents, and the cones form an unexpectedly high 10% proportion of the photoreceptors. Of these, S-cones constitute a regionally varying proportion from 2% in dorsal to 20% in ventral retina. The high cone proportion suggests adaptation to visual demands during the sporadic short phases of diurnal surface activity, rather than to the lightless subterranean environment. Our measurements on fresh cururo urine reveal a high UV reflectance, suggesting that scent marks may be visible to the UV-sensitive cones. The present results challenge the general view of convergent adaptive eye reduction and blindness in subterranean mammals.
Since their discovery, naked mole-rats have been speaking to us. Early field studies noted their extensive vocalizations, and scientists who are fortunate enough to spend time with these creatures in the laboratory setting cannot help but notice their constant peeping, chirruping and grunting (Hill et al., Proc Zool Soc Lond 128:455–514, 1957). Yet, few dwell on the function of these chirps and peeps, being instead drawn to the many other extraordinary aspects of naked mole-rat physiology detailed throughout this book. Still, no biology is complete without a description of how an organism communicates. While the field of naked mole-rat bioacoustics and acoustic communication has been largely silent for many years, we highlight recent progress in understanding how and what Heterocephalus glaber hears and which vocalizations it uses. These efforts are essential for a complete understanding of naked mole-rat cooperation, society and even culture.
In the world agriculture and civilization, wheat is one of the most important crops. The major factor underlying human civilization is domestication of plants and animals. Cultivated wheat includes the hexaploid bread wheat (Triticum aestivum) and the tetraploid durum wheat (Triticum durum). About 10,000 years ago, T. aestivum derived from a cross between domesticated emmer (Triticum dicoccum) and the goat grass Aegilops tauschii. Wild emmer wheat (Triticum dicoccoides) is the progenitor of cultivated wheat and has played core role to wheat domestication that has genetically not only transformed the brittle rachis, tenacious glume and nonfree threshability but also modified yield and yield components. T. dicoccoides harbors many useful genes conferring many agronomic traits, abiotic stress tolerances, biotic stress resistances, grain protein content, processing quality, and micronutrient mineral concentrations. Domestication of T. dicoccoides is actually related with a few chromosome regions or domestication syndrome factors. Whole genome sequences of T. dicoccoides and other Triticum species could be helpful for isolation of genes controlling important traits. However, the majority of genetic resources in T. dicoccoides still remain untapped. The large number of molecular markers, fully annotated genome sequences, and efficient cloning techniques will greatly accelerate application of T. dicoccoides germplasm to wheat improvement programs and ensure sustainability of global wheat production.
Rodents live in a wide variety of habitats all over the world. They are known to use vocalizations for communication, requiring good auditory acuity to detect, discriminate, identify, and localize these vocalizations. Most of the work measuring auditory acuity as a function of species, age, and sex has been conducted on laboratory mice and rats. These measurements can be used as baseline functions to determine the effects of hormones on hearing and the auditory system in general. Hormones such as glucocorticoids, mineralocorticoids, estrogen, insulin-like growth factor-1, and thyroid hormone have roles in the development of the auditory system, protection of the aging auditory system, and the restoration of hearing after trauma. More studies are needed to determine whether the findings from laboratory animals translate to wild rodents living in various environments with differing ecological characteristics and evolutionary pressures.
Hearing in rodents has been measured using both behavioral and physiological methods. Features of hearing that have been measured in rodents include auditory acuity in quiet and in noise, frequency selectivity and sensitivity, intensity resolution, temporal resolution, and complex sound perception. Generally, and especially for simple tone detection, behavioral thresholds are lower than physiological thresholds. Within behavioral studies, operant experiments using awake, behaving rodents produce lower thresholds than simple reflexive measures. Rodents generally have broader frequency filters than other mammals. Frequency and intensity resolution are similar but slightly elevated relative to other mammals. The few measures of complex sound perception performed to date show that at least some rodents have the capacity to distinguish between spectrotemporal characteristics of acoustic signals for communication. Most studies have typically employed domesticated laboratory rodents rather than wild-caught species, so few attempts have been made to correlate lifestyle and evolutionary history with auditory processing. Nonetheless, a baseline knowledge of hearing abilities in rodents will facilitate experiments on the perception of more complex, natural acoustic stimuli in the future.
Ecological restrictions of the subterranean environment have resulted in sensory adaptations in its inhabitants that limit communication below ground. Adaptations such as degenerate vision and reduced hearing capabilities influence the communicative methods employed by subterranean rodents. Due to the logistic difficulties of investigating life underground, little is known about subterranean rodent communication. Vocal repertoires have been examined in a limited number of subterranean species, but never in North American taxa. We examined vocal communication in Baird's Pocket Gopher Geomys breviceps, a species indigenous to south central North America. Our results show that this species has a repertoire of 4 audible signals, 2 of which are only emitted during close-contact encounters. Energy of signals was concentrated within the frequency range correlating with pocket gophers' greatest hearing sensitivity. Results are also consistent with the frequency requirements for efficient transmission in the subterranean environment. Corresponding behavioural contexts suggest that vocal communication is important for facilitating social interaction with G. breviceps. Because the Geomyidae extend the furthest into the fossil record and are exclusively solitary species, this group is of fundamental importance for considering evolution of communication in subterranean rodents.
We studied the inner ear of Ctenomys talarum, a small solitary subterranean rodent distributed in the southern region of Buenos Aires Province (Argentina) using standard staining techniques. The inner ear of this subterranean rodent is characterized by a long basilar membrane, a higher density of cochlear receptors in the apical region of the basilar membrane and a gradual increment of the width of the triad of outer hair cells from the base towards the apex. These anatomical features of the cochlea of C. talarum can be interpreted as biomechanical specializations to enhance low-frequency sound reception.
The maintenance of social relationships is critical for group-dwelling species. Social animals often exhibit behaviors such as antiphonal vocalizations that reduce conflict and maintain affiliations. Naked mole-rats (Heterocephalus glaber) have a complex hierarchical society comparable to that of bees and ants. They are also known for their extensive vocal repertoire, which may have evolved in the absence of visual cues. The most frequent vocalization used by naked mole-rats is the soft chirp (SC). It has an antiphonal nature and may function in rank identification and in maintaining affiliations. Relative body weight differences, which are directly related to social rank, are positively correlated with SC emission rates. SCs are elicited from either physical touch or the SC of another conspecific, and other cues might contribute to SC utterance. In the current study, we examined whether an SC alone was able to elicit SC responses. Specifically, we presented artificial SC-like sounds and determined whether the response rate was modulated by the acoustic properties of the stimulus. An analysis of response latency revealed that animals responded to the audio stimuli, and a single audio stimulus could elicit responses from two animals. Thus, antiphony in naked mole-rats may occur among three or more animals. We also found that animals were able to discriminate the acoustic properties of the stimulus and responded more frequently to audio stimuli resembling SCs from large animals than to those resembling SCs from small animals. Therefore, naked mole-rats may be able to judge social relationships (dominant or subordinate) based solely on SCs. The constraints of subterranean habitats and increased social complexity may have led to the evolution of this communication system.
We studied the middle and inner ears of seven adult coruros (Spalacopus cyanus), subterranean and social rodents from central Chile, using free-hand dissection and routine staining techniques. Middle ear parameters that were focused on here (enlarged bullae and eardrums, ossicles of the "freely mobile type") are believed to enhance hearing sensitivity at lower frequencies. The organ of Corti was of a common mammalian type and revealed three peaks of higher inner hair cell densities. Based on a position frequency map, frequencies were assigned to the respective peaks along the basilar membrane. The first peak at around 300-400 Hz is discussed with respect to the burrow acoustics, while the peak around 10-20 kHz is probably a plesiomorphic feature. The most pronounced peak at around 2 kHz reflects the frequency at which the main energy of vocal communication occurs. The morphology of the ear of the coruro corresponds to the typical pattern seen in subterranean rodents (low frequency and low-sensitivity hearers), yet, at the same time, it also deviates from it in several functionally relevant features.
Absolute and frequency‐difference thresholds were determined by the conditioned‐suppression technique. The results show that the average frequency range of audibility at +50 dB sound‐pressure level extends from 86 Hz to 46.5 kHz, with a best frequency near 8 kHz. Individual differences in sensitivity are related to body weight and, probably, age. The average frequency‐difference limen is 3.5% from 125 Hz to 42 kHz. Compared to other mammals, the auditory capacities of guinea pig are within one standard deviation of the mammalian mean on each of six dimensions: high‐frequency and low‐frequency cutoff, lowest intensity, best frequency, area of the audible field, and frequency discrimination.
Coruros Spalacopus cyanus, social fossorial rodents from Chile, use a complex acoustic repertoire with eleven different true vocalisations and one mechanical sound in various behavioural contexts. The complex of contact calls is particularly well differentiated. Juvenile coruros produced six true vocalisations of which four were structurally identical to adult calls. One vocalisation had components of two adult sounds and one occurred only in juvenile animals. Certain calls from the adult repertoire were lacking. The frequencies of sounds of juveniles were considerably higher than those of adults, with many sounds reaching the ultrasonic range. Nevertheless, pure ultrasonic sounds were not recorded.The frequencies of the analysed sounds of coruros extended from 0.17 to 20.33 kHz with dominant frequency components between 0.17 and 10 kHz. The acoustic properties of calls are suitable for transmission above and below ground, thus providing further indirect evidence that coruros are not strictly confined to an underground way of life. Indeed, the great variability of frequency ranges, with lower frequencies always being included, reflects a specialisation for communication in variable acoustic environments.The most distinctive and unique vocalisation of coruros is the long duration musical trilling (lasting up to two minutes), which is a long-distance call emitted in alarm and arousal contexts. Recordings of this call from natural burrows in the field in Chile showed similar structural features to vocalisations from captive colonies in the laboratory.Our findings provide a further example of matching physical properties of vocalisations to the acoustic conditions of the habitat. However, vocalisations in subterranean rodents consist almost exclusively of short-distance calls, the trilling of coruros being the notable exception. Since the selective pressure of the acoustic environment upon the evolution of short-distance vocalisations is probably minimal, we suggest that during their evolution, subterranean mammals have matched their vocalisations primarily to their hearing range and not directly to the acoustics underground. Hearing probably has been the primary target of natural selection, serving not only for communication but also for detection of predators (and, in carnivores, of prey).
The first information on the reproductive biology and development of the fossorial and social coruro (Spalacopus cyanus), obtained in the field and through study of captive animals, is reported herein. Signs of sexual and reproductive activity were found in 26% (n = 88) of males and 44% (n = 99) of females collected in Chile from March through January. The largest colony of 26 animals included four pregnant females. Gestation (established in captivity) was 77 days; mean litter size (3.5 ± 1.4 SD, range 2-5) agreed with the litter sizes based on placental scars and embryo counts from field-caught animals. The sex ratio was comparable for field-caught non-breeding (subadult) animals and neonates in captivity and approached 1.2 male: 1 female. The sex ratio for reproductive (adult) field-caught animals was 0.5:1. The average body weight for neonates in captivity was 8.9 g. Eyes opened at 2-8 days when neonates weighed ca. 9.7 g. Pups were weaned after 2 months at body weights of ca. 47 g. Adult weight in captivity (106 ± 7 g in males and 95 ± 18 g in females) was attained at ca. 6-7 months.
Determined behavioral audiograms for 3 horses and 2 cows. Horses' hearing ranged from 55 Hz to 33.3 kHz, with a region of best sensitivity from 1 to 16 kHz. Cattle hearing ranged from 23 Hz to 35 kHz, with a well-defined point of best sensitivity at 8 kHz. Of the 2 species, cattle proved to have more acute hearing, with a lowest threshold of –21 db (re 20 μN/m–2) compared with the horses' lowest threshold of 7 db. Comparative analysis of the hearing abilities of these 2 species with those of other mammals provides further support for the relation between interaural distance and high-frequency hearing and between high- and low-frequency hearing. (39 ref) (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Behavioral audiograms were determined for four species of Glires: one lagomorph (domestic rabbit, O r y c t o l a g u s c u n i c u l u s) and three feral rodents (cotton rat, S i g m o d o n h i s p i d u s; house mouse, M u s m u s c u l u s; and kangaroo rat, D i p o d o m y s m e r r i a m i). Considerable variation in hearing ability was found among the four species with low‐frequency hearing limits ranging over 5‐1/2 octaves from 50 (kangaroo rat) to 2300 Hz (feral mouse) and high‐frequency hearing limits ranging from 49 (rabbit) to 90 kHz (feral mouse). Comparison of the characteristics of each audiogram with the audiograms of other animals of the same Order, Cohort, and Class provide further evidence for the validity of two relationships: (1) interaural distance is strongly and inversely correlated with high‐frequency hearing ability, and (2) good high‐frequency hearing is apparently incompatible with good low‐frequency hearing in most, if not all, land mammals. Furthermore, it is shown that cotton rats and feral mice possess the ability to perform frequency discriminations even at very high frequencies, indicating that there is probably no difference about the way in which they perceive high and low‐frequency sounds. Finally, it is shown that kangaroo rats are not unusual in their ability to localize brief sounds, indicating that these animals have not compromised this ability in their acquistion of their unusual low‐frequency sensitivity.
Daily patterns of activity were studied under laboratory conditions in 12 coruros, Spalacopus cyanus, subterranean social rodents originally from Chile. When able to burrow, coruros spent 90% of the total time underground, and surface activity occurred during the 1st hours of darkness. When prevented from burrowing, locomotory activity of coruro groups peaked near the onset of darkness but also occurred during episodes of light. Individually housed coruros displayed a clear nocturnal activity pattern. Coruros exhibited endogenous circadian rhythms entrained by a light–dark cycle.
Two blind mole rats were tested for their ability to detect and localize sound. The results indicate that blind mole rats have severely limited, and probably degenerate, auditory abilities. Although their 60-dB low-frequency hearing limit of 54 Hz is within the range for other rodents, the highest frequency they can hear at a level of 60 dB SPL is only 5.9 kHz, giving them the poorest high-frequency sensitivity yet observed in any mammal. In addition they have poor sensitivity as indicated by the fact that their lowest threshold is only 32 dB SPL (at 1 kHz). Finally, they are unable to localize brief sounds but retain a rudimentary ability to localize sounds of 0.5 s or longer. These results, combined with those of previous studies of subterranean species (i.e., blind mole rats, naked mole rats, and pocket gophers), suggest that poor auditory sensitivity, the loss of high-frequency hearing, and an inability to localize brief sounds is a degenerate state which may be characteristic of subterranean mammals. Thus it appears that an exclusive adaptation to a subterranean lifestyle (where airborne sound propagates poorly and where directional responses are limited by the tunnels) can result in vestigial auditory abilities just as the absence of light results in vestigial vision.
The cochlea of the mole rat Cryptomys hottentotus was investigated with physiological and anatomical methods. In order to reveal the place-frequency map of the cochlea, iontophoretic HRP-applications were made in the cochlear nucleus at physiologically characterized locations. Subsequent HRP-transport in auditory nerve fibres and labeling patterns of spiral ganglion cells within the cochlea were evaluated.
A cochlear place-frequency map was constructed from 17 HRP-applications in the cochlear nucleus at positions where neurons had characteristic frequencies between 0.1 and 12.6 kHz. As in other mammals, high frequencies were found to be represented at the cochlear base, low frequencies at the cochlear apex. The placefrequency map had three distinct parts which were characterized by their different slopes. A clear overrepresentation of the frequencies between 0.6 and 1 kHz was revealed, in this frequency range the slope of the place-frequency map amounted to 5.3 mm/octave. As calculated from the regression analysis, below 0.6 kHz the slope of the cochlear place-frequency map amounted to 0.24 mm/octave, above 1 kHz to 0.9 mm/octave.
As in other mammals width of the basilar membrane (BM) increased from the cochlear base towards the cochlear apex. Also in concordance with the findings in other mammals, BM-thickness decreased from the cochlear base to the apex. However, it was remarkable to find that there was no or little change in BM-width and thickness between 40 and 85% BM-length. It was also revealed that scala tympani was only 1/10th the size found in the rat or other mammals of similar body size.
On the basis of the cochlear place-frequency map and the morphological findings we speculate that in Cryptomys hottentotus an acoustic fovea is present in the frequency range between 0.6 and 1 kHz. In analogy to echolocating bats, about half of the cochlea is devoted to the analysis of a narrow frequency band within the hearing range.
The audiograms of two wood rats and three grasshopper mice were determined with a conditioned avoidance procedure. The wood rats were able to hear tones from 940 Hz to 56 kHz at a level of 60 dB (SPL), with their best sensitivity of -3 dB occurring at 8 kHz. The hearing of the grasshopper mice ranged from 1.85 kHz to 69 kHz at 60 dB (SPL), with their best sensitivity of 9 dB also occurring at 8 kHz. These results support the relation between interaural distance and high-frequency hearing and between high- and low-frequency hearing. The inability of the grasshopper mouse to hear low frequencies as well as other desert rodents such as kangaroo rats and gerbils demonstrates that not all rodents found in deserts have developed good low-frequency hearing. The degree to which general and specific selective pressures have played a role in the evolution of rodent hearing is discussed.
Absolute and frequency-difference thresholds were determined by the conditioned-suppression technique. The results show that the average frequency range of audibility at +50 dB sound-pressure level extends from 86 Hz to 46.5 kHz, with a best frequency near 8 kHz. Individual differences in sensitivity are related to body weight and, probably, age. The average frequency-difference 1/men is 3.5% from 125 I-Iz to 42 kHz. Compared to other mammals, the auditory capacities of guinea pig are within one standard deviation of the mammalian mean on each of six dimensions: high-frequency and low-frequency cutoff, lowest intensity, best frequency, area of the audible field, and frequency discrimination.
The behavioral audiogram of the hooded Norway rat was determined for frequencies from 250 Hz to 70 kHz. The resulting audiogram is virtually identical to the albino rat audiogram obtained by Kelly and Masterton (1977), indicating that there is no detectable effect of albinism on the audiogram of the Norway rat. The two audiograms also indicate the degree of replicability that can be obtained with current behavioral techniques.
Behavioral audiograms were determined for four black-tailed and one white-tailed prairie dogs (Cynomys ludovicianus and C. leucurus) using a conditioned avoidance procedure. The hearing of black-tailed prairie dogs ranges from 29 Hz to 26 kHz and that of the white-tailed prairie dog from 44 Hz to 26 kHz (at sound pressure levels of 60 dB). Both species have good low-frequency hearing, especially black-tailed prairie dogs which can hear as low as 4 Hz and are more sensitive than any other rodent yet tested at frequencies below 63 Hz. In contrast, prairie dogs are relatively insensitive in their midrange and have poor high-frequency hearing. It is suggested that the reduced midrange sensitivity and high-frequency hearing are related to their adaptation to an underground lifestyle with its reduced selective pressure for sound localization. In this respect they appear to be intermediate between the more exclusively subterranean rodents (such as gophers and mole rats) and surface dwellers (such as chinchillas and kangaroo rats).
The chapters of this volume review what is understood about the similarities and differences among mammals in their sense of hearing, defined behaviorally, and the structures of the ear that condition and transform sound wave-forms before they are transduced into patterns of neural activity.
Calls used during courtship were analyzed for 59 male mole rats (Spalax ehrenbergi). The x̄ ± SD of the main frequency was 568.0 ± 35.6 Hz, the lower value of the main frequency according to sonograms was 502.3 ± 36.9 Hz, and the pulse repetition rate was 23.7 ± 2.8/s. Calls are noisy, with energy spread primarily from 0.5 to 4.5 kHz. The low frequency of this call seems to be a specialization to life in underground tunnels.
In the coastal region of central Chile the coruro, Spalacopus cyanus, lives in large populations consisting of many small, nomadic colonies. One colony contained 15 members belonging to no less than three generations. A colony of coruros occupies a common burrow system and apparently wanders continuously in search of food. Coruros feed primarily, if not exclusively, on the tubers and underground stems of the lily, Leucoryne ixiodes. S. cyanus has a higher metabolic rate than similar-sized fossorial species of Ctenomys. In February, adult males were sexually active and two of six adult females were pregnant, each bearing three small fetuses.
Burrow systems of two coastal populations (El Alamo and Los Maitenes) of the social octodontid rodent Spalacopus cyanus were studied in central Chile. Tunnel systems were estimated to be up to 600 m long, ran at a depth of 15 cm and had a diameter of 6 cm. Tunnel openings were usually unplugged, and a minor preference toward southern and south-eastern direction of entrances was apparent. Nests, frequently found in the root system of Berberis actinacantha at a depth of 30 cm, consisted of grasses, roots and plastic bags. Nests serve for sleep, care of the pups and as latrines. Many staphylinid beetles of the genus Edrabius and other invertebrates were found in the breeding nests. Food chambers contained up to 13.2 kg of bulbs of the geophyte Dioscorea longipes collected by a single colony consisting of 26 animals (including 10 adults) and were frequently found at El Alamo. However, no bulbs were found at Los Maitenes, where the coruros forage above ground on leaves of Convolvulus arvensis within a radius of about 10 cm of the entrances. Apparently, the burrow design is also affected by food availability, soil quality, and colony size.
Behavioral tests of absolute sensitivity and sound localization in African naked mole rats show that, despite their communal social structure and large vocal repertoire, their hearing has degenerated much like that of other subterranean species. First, their ability to detect sound is limited, with their maximum sensitivity being only 35 dB (occurring at 4 kHz). Second, their high-frequency hearing is severely limited, with their hearing range (at 60 dB sound pressure level [SPL]) extending from 65 Hz to only 12.8 kHz. Third, determination of the effect of duration on noise thresholds indicates that, compared with other animals, mole rats require a sound to be present for a much longer duration before reaching asymptotic threshold. Finally, they are unable consistently to localize sounds shorter than 400 ms and cannot accurately localize sounds of longer duration, raising the possibility that they are unable to use binaural locus cues. Thus, it seems that the essentially one-dimensional burrow system of a subterranean habitat produces severe changes in hearing comparable to the changes in vision that result from the absence of light. To explore the relation between vision and sound-localization acuity, retinal ganglion cell densities were determined. The results indicate that naked mole rats have a broad area of best (albeit poor) vision, with maximum acuity estimated at 44 cycles/degree. That mammals with wide fields of best vision have poorer sound-localization acuity than those with narrower fields is consistent with the thesis that a major function of sound localization is to direct the gaze to the source of a sound. However, the fact that subterranean mammals have little use for vision in a lightless environment suggests that they represent an extreme case in this relationship and may explain the fact that, unlike surface-dwelling mammals, they have virtually lost the ability to localize brief sounds. Finally, despite their very limited auditory abilities, the major brainstem auditory nuclei, although relatively small, appear to be present. © 1993 Wiley-Liss, Inc.
Thesis (doctoral)--Universität-GH Essen, 1999.
Compared to acoustically unspecialized mammals (soricids and murids), the middle ear of subterranean insectivores and rodents (twelve species of six families examined) was clearly distinguished and characterized by many common features: rather round and relatively larger eardrum without a pars flaccida; reduced gonial; loose or no connection between the malleus and the tympanic bone; reduced and straightened transversal part of the malleus; enlarged incus; increased and rather flat incudo-mallear joint; rather parallel position of the mallear manubrium and incudal crus longum in some species (and their fusion in bathyergids); reduced or even missing middle ear muscles. Convergent occurrence of these structural features in taxa of different origin and their generally derived character suggest that they cannot be categorized as degenerative. The form of the stapes can be considered as a non-adaptive trait; it was taxon specific yet remarkably polymorphous in some species and exhibited no convergent features among subterranean mammals. Structural retrogression resulting in a columella-like stapes was observed in some species lacking the stapedial artery. The stapedial base was relatively larger than in unspecialized mammals. The subterranean mammals did not exhibit conspicuously enlarged eardrums as would be required for sensitive tuning to low frequencies. It is, however, argued that while selective pressures in the subterranean ecotope promoted hearing of low frequencies, hearing sensitivity did not have to be enhanced.
Behavioral tests of hearing and sound localization in the North American pocket gopher (Geomys bursarius) show that it is unique among mammals. It has a severely attenuated range of hearing and only rudimentary ability to localize sound. In these respects, the hearing of gophers can be properly termed 'vestigial' and suggests that life underground can produce as severe a change in hearing as a light-less world produces in vision or an odorless world produces in olfaction.
The adaptive value of sound signal characteristics for transmission in the underground tunnel ecotope was tested using tunnels of the solitary territorial subterranean mole rats. We analyzed the propagation of synthetic calls with various frequencies through natural tunnels along different distances. Here we present evidence that sound propagation proved efficient only across short distances (a few meters). The least attenuation of sounds occurred at low frequencies. The 440 Hz sound was transmitted better than the lower (220 Hz) or higher (880, 1760, 3520 Hz) tested frequencies. These characteristics matched perfectly with the mole rat features of vocalization and hearing, thus reflecting the operation of natural selection for adaptive vocal communication in the underground tunnel ecotope.
The measurement of distortion-product otoacoustic emissions is a noninvasive method that can be used for assessing the sensitivity and the frequency tuning of nonlinear cochlear mechanics. During stimulation with two pure tones f1 and f2, the acoustic 2f1-f2 distortion was recorded in the ear canal of Cryptomys spec. to study specializations in cochlear mechanics that could be associated with the presence of a frequency expanded cochlear region between 0.8–1 kHz. In addition, a distortion threshold curve was obtained which describes relative threshold of nonlinear cochlear mechanics. Sensitive distortion thresholds could be measured for stimulus frequencies between 0.4 to 18 kHz with a broad minimum between 0.75 to 2.5 kHz. The distortion threshold curve extends to higher frequencies than previous neuronal data indicated.
As a measure of mechanical tuning sharpness in the cochlea, suppression tuning curves of 2f1-f2 were recorded. The tuning curves reflected the typical mammalian pattern with shallow low frequency and steep high frequency slopes. Their tuning sharpness was poor with Q10dB values between 0.3 and 1.88. In the range of the frequency expanded region, the Q10dB values were below 0.5. This finding emphasizes that the presence of frequency expansion does not necessarily lead to enhanced mechanical tuning in the cochlea and one has to consider if in certain bat species with cochlear frequency expansion and particularly sharp cochlear tuning, the two phenomena may not be interlinked.
In captive adult Zambian mole-rats 14 different sounds (13 true vocalizations) have been recorded during different behavioural contexts. The sound analysis revealed that all sounds occurred in a low and middle frequency range with main energy below 10 kHz. The majority of calls contained components of 1.6-2 kHz, 0.63-0.8 kHz, and/or 5-6.3 kHz. The vocalization range thus matched well the hearing range as established in other studies. The frequency content of courtship calls in two species of Zambian Cryptomys was compared with that in naked mole-rats (Heterocephalus glaber) and blind mole-rats (Spalax ehrenbergi) as described in the literature. The frequency range of maximum sound energy is negatively correlated with the body weight and coincides with the frequencies of best hearing in the respective species. In general, the vocalization range in subterranean mammals is shifted towards low frequencies which are best propagated in underground burrows.
Thresholds for pure tone detection were examined in the common mole-rat, Cryptomys sp. (Bath-yergidae, Rodentia) using a positive reinforcement procedure. To bypass the problems connected with testing isolated individuals of this extremely social species, a collective behavioural audiogram was determined for a family group of seven mole-rats. Within the tested frequency range of 225 to 18 kHz, the lowest thresholds (as low as 7.5 dB SPL, on average 24 dB SPL) were found at 800 Hz, the upper limit of hearing (at the level of 60 dB SPL) was at 18 kHz. The behavioural audiogram combines the results of previous studies on hearing in this species. It resembles the distortion threshold curve but differs from neurophysiological data as far as the high frequency cutoff is concerned. On the other hand, the region of the best hearing sensitivity is narrow in behavioural audiogram and neurophysiological curves but rather broad in the distortion threshold curve. In general, the behavioural audiogram of Cryptomys is in many aspects comparable with the available audiograms of other subterranean rodents.
Vocali-zation of the naked mole-rat
- Jw
- Braude
- Lacey Ea Sh
- Sherman
- Pw
Regression, progression, and global convergence. Oxford Uni-versity Press Inc., New York Pepper JW, Braude SH, Lacey EA, Sherman PW (1991) Vocali-zation of the naked mole-rat. In: Sherman PW, Jarvis JUM, Alexander RD (eds) The biology of the naked mole-rat.
Acoustic communication underground: vocalization characteristics in subterranean social mole-rats (Cryptomys sp., Bathyergidae) Comparative auditory research Behavioural audiometry in mammals: Review and evaluation of techniques
- S H Burda
- Ludescher
S, Burda H, Ludescher F (1997) Acoustic communication underground: vocalization characteristics in subterranean social mole-rats (Cryptomys sp., Bathyergidae). J Comp Physiol A 180:245–255 Fay RR (1994) Comparative auditory research. In: Fay RR, Popper AN (eds) Comparative hearing: mammals. Springer handbook of auditory research, vol 4. Springer, Berlin Heidel-berg New York, pp 1–17 Francis RL (1975) Behavioural audiometry in mammals: Review and evaluation of techniques. Symp Zool Soc Lond 37:237–289
Feeding ecology of the barn owl (Tyto alba) in central Chile and its relation to the hunting habitat
- S Begall
Begall S (1999) Verhaltenso¨kologische und genetische Analysen der
Sozial-und Populationsstruktur von Coruros (Spalacopus cyanus, Octodontidae, Rodentia) aus Chile. PhD thesis, Faculty
of Biosciences, University of Essen
Begall S (in press) Feeding ecology of the barn owl (Tyto alba) in
central Chile and its relation to the hunting habitat. J Raptor
Res
Begall S, Gallardo MH (2000) Spalacopus cyanus (Octodontidae,
Rodentia): an extremist in tunnel constructing and food storing
among subterranean mammals. J Zool Lond 251:53-60
Comparative auditory research Comparative hearing: mammals. Springer handbook of auditory research
- Rr Fay
Vocalization of the naked mole-rat The biology of the naked mole-rat
- Jw Pepper
- Sh Braude
- Ea Lacey
- Pw Sherman
Los pequen˜os mamı´feros de Chile. Gayana: Zoo-logı´a 40
- G Mann
Mann G (1978) Los pequen˜os mamı´feros de Chile. Gayana: Zoo-logı´a 40. Universidad de Concepcio´n, Chile